Seeding date and location affect winter wheat infection by common bunt (Tilletia tritici and T. laevis) in western Canada

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1 Seeding date and location affect winter wheat infection by common bunt (Tilletia tritici and T. laevis) in western Canada D. A. Gaudet 1, B. J. Puchalski 1, T. Despins 1, C. McCartney 2,4, J. G. Menzies 3, and R. J. Graf 1 1 Agriculture and Agri-Food Canada, Lethbridge Research Centre, st Avenue South, Lethbridge, Alberta, Canada T1J 4B1; 2 Crop Development Centre, University of Saskatchewan, 51 Campus Drive, Saskatoon, Saskatchewan, Canada S7N 5A8; and 3 Agriculture and Agri-Food Canada, Cereal Research Centre, 195 Dafoe Road, Winnipeg, Manitoba, Canada R3T 2M9. Received 20 July 2012, accepted 7 December Gaudet, D. A., Puchalski, B. J., Despins, T., McCartney, C., Menzies, J. G. and Graf, R. J Seeding date and location affect winter wheat infection by common bunt (Tilletia tritici and T. laevis) in western Canada. Can. J. Plant Sci. 93: The majority of western Canadian winter wheat varieties are susceptible to common bunt (Tilletia tritici and T. laevis) and the risk to production, particularly in Saskatchewan and Manitoba, where the majority of production occurs, is unknown. Inoculated trials were employed to determine the effects of fall seeding date on bunt infection levels on one resistant and two susceptible winter wheat varieties at three locations in western Canada during three growing seasons from 2007/2008 to 2009/2010. Among the three locations, average infection levels were highest in Lethbridge, AB, followed by Glenlea, MB, and Saskatoon, SK. Later seeding resulted in high infection levels at all three locations in the susceptible varieties, particularly in Lethbridge, but high infection levels were observed in the earliest seeded treatments at both the Saskatchewan and Manitoba locations. The resistant variety Blizzard consistently exhibited infection levels of less than 3% infection across all environments. In a second test at conducted at Lethbridge, 10 of the 11 currently grown winter wheat varieties were susceptible to common bunt. These results indicate that there is a general risk of common bunt infection to winter wheat production across western Canada and that control measures must be taken until resistant varieties are developed. Key words: Common bunt, wheat (winter), seeding date, Bt genes Gaudet, D. A., Puchalski, B. J., Despins, T., McCartney, C., Menzies, J. G. et Graf, R. J La date et l emplacement des semis affectent l infection du ble d hiver par la carie (Tilletia tritici et T. laevis) dans l Ouest canadien. Can. J. Plant Sci. 93: La plupart des varie tés canadiennes de ble d hiver sont sensibles a` la carie (Tilletia tritici et T. laevis) et on ignore les risques que cela pose pour la production, surtout dans les re gions ou` l on cultive le plus le ble, comme la Saskatchewan et Manitoba. Les auteurs ont procéde a` des essais d inoculation pour tenter d e tablir de quelle manie` re la date des semis automnaux peut influer sur le degre d infection par la carie pour une varie té de ble d hiver re sistante et deux sensibles. Les essais se sont de roule s a` trois endroits, dans l Ouest canadien, pendant trois saisons ve gétatives (de a` ). Des trois sites, c est celui de Lethbridge, en Alberta, qui était le plus atteint, en moyenne; suivaient Glenlea, au Manitoba, et Saskatoon, en Saskatchewan. Des semis plus tardifs engendrent un taux d infection éleve des varie te s sensibles, aux trois endroits, mais on a observé un degre d infection éleve avec les semis les plus haˆtifs, en Saskatchewan et au Manitoba. La varie té résistante Blizzard a toujours profite d un taux d infection inférieur a` 3 %, peu importe l environnement. Lors d un deuxie` me essai, re alise à Lethbridge, 10 des 11 varie te s de ble d hiver actuellement cultive es se sont ave rées sensibles a` la carie. Ces résultats indiquent qu il existe un risque ge néral de voir le ble d hiver attaque par la carie partout dans l Ouest canadien et qu il faut adopter des mesures pour y reme dier jusqu a` ce que des varie te s re sistantes aient e te mises au point. Mots clés: Carie, ble (d hiver), date des semis, ge` nes Bt Common bunt, incited by Tilletia tritici (Bjerk.) Wint. [syn. Tilletia caries (DC.) Tul.] and T. laevis Ku hn [syn. T. foetida (Wallr.) Liro.], caused extensive losses in spring and winter wheat (Triticum aestivum L. em. Thell) in western Canada prior to 1940 (Cherewick 1953). 4 Present Address: Agriculture and Agri-Food Canada, Cereal Research Centre, 195 Dafoe Road, Winnipeg, Manitoba, Canada R3T 2M9. The disease is caused by seed and soil-borne teliospores that germinate and infect the developing seedling; the fungus develops systemically in the plant and produces spore containing bunt balls that eventually replace the kernel (Cherewick 1953; Hoffmann 1982). Although yield loss is directly proportional to the number of bunted Abbreviations: CWRS, Canada Western Red Spring; CPS, Canada Prairie Spring Can. J. Plant Sci. (2013) 93: doi: /cjps

2 484 CANADIAN JOURNAL OF PLANT SCIENCE heads (Slinkard and Elliott 1954), far greater financial losses are the result of grade reduction or complete rejection of the grain, a result of the pungent fishy odour imparted to the grain at infection levels as low as 0.05% by weight (Bailey et al. 2003). Early Canadian hard red spring and durum wheat cultivars were susceptible to common bunt (Hanna and Popp 1930; Cherewick 1953), but the majority of the varieties currently grown in the dominant Canada Western Red Spring (CWRS) market class possess intermediate to high levels of race non-specific resistance, while the registered durum wheat cultivars are uniformly highly resistant and may possess race specific genes (Gaudet and Puchalski 1989a). Nonetheless, some western Canadian wheat cultivars across the various market classes [CWRS, Canada Prairie Spring (CPS) Red, Canada Western Soft White Spring] are susceptible (Gaudet and Puchalski 1989a). Western Canadian winter wheat varieties remain susceptible to common bunt, and localized outbreaks occur occasionally (Horricks and Moffatt 1958). At present, most of the resistance in CWRS and CPS wheat varieties rely on the single, race-specific gene Bt-10 and/or Hope resistance (Gaudet and Puchalski 1989a; Fofana et al. 2008). Soil temperature is the most important of the numerous environmental factors that can affect the severity of common bunt (Leukel 1937; Goates 1996). Soil temperatures between 6 and 108C at seeding favour infection and, thus, early seeding of spring wheat and late seeding of winter wheat into cool soils increases the risk of bunt infection (Holton and Heald 1941; Purdy and Kendrick 1957; Gaudet and Puchalski 1990; Gaudet et al. 1994; Gaudet and Puchalski 1995). As a consequence of this low temperature requirement for teliospore germination, delayed seeding of spring wheat (Gaudet and Puchalski 1995) and early seeding of winter wheat (Fischer and Holton 1957; Purdy and Kendrick 1957) have been shown to be detrimental to infection. Southern Alberta is considered the traditional winter wheat region for western Canada but in recent years there has been widespread adoption of the crop in Saskatchewan and Manitoba, to the extent that 71% of the ha sown in 2010 were outside of Alberta (Statistics Canada 2011). The risk of common bunt Table 1. Seeding dates at Lethbridge, Saskatoon and Glenlea infection of winter wheat in Saskatchewan and Manitoba is unknown due to the relatively recent adoption of winter wheat in these provinces. The present field study was conducted at three locations in western Canada to determine the effect of environment on the level of bunt infection when winter wheat varieties varying in resistance level were sown at different dates. Additionally, bunt infection levels were established for the varieties commonly grown in western Canada. This information will be relevant for extension agronomists and plant breeders for understanding the risk of bunt infection in winter wheat grown in western Canada and the level of resistance of potential parents in order to effectively incorporate high levels of stable resistance into future varieties. MATERIALS AND METHODS Seed for all tests was inoculated with a composite of races that consisted of T-1, T-6, T-13, and T-19 of T. tritici and L-7 and L-16 of T. laevis in a 1:1:1:1:2:2 ratio (vol/vol), respectively, with the excess inoculum removed by shaking the seed over a fine mesh sieve according to Gaudet and Puchalski (1989a). The combined virulence of these races is known to overcome the bunt resistance genes Bt1, 2, 3, 4, 6, and 7 (Gaudet and Puchalski 1989b). Seed was sown 5 cm deep at 10 g per 5 m row, which served as a plot. Test 1 was conducted for 3 yr, from 2007/2008 to 2009/2010 at an irrigated site at the Agriculture and Agri-Food Canada (AAFC) Lethbridge Research Centre, Lethbridge, AB, the University of Saskatchewan s North Seed Farm, Saskatoon, SK, and the AAFC Glenlea Research Farm, Glenlea, MB (Table 1). Within each site, plots were seeded in different areas during the three years to prevent soil-borne contamination. In order to prevent contamination between inoculated and non-inoculated treatments, the seeder was thoroughly sanitized with 70% ethanol between seeding dates. Additionally, for each seeding date, the replicates involving non-inoculated treatments were seeded before those of the inoculated treatments. The varieties Radiant (Thomas et al. 2012a), CDC Osprey (Fowler 1997) and Blizzard (Sunderman et al. 1991) were employed: Radiant and CDC Osprey are currently registered for production in western Canada and known to be Location Lethbridge Saskatoon Glenlea Year /2008 Sep. 06 Sep. 18 Oct. 02 Sep. 06 Sep. 18 Oct. 02 Sep. 04 Sep. 18 Oct /2009 Aug. 27 Sep. 17 Oct. 08 z 2009/2010 Aug. 25 Sep. 14 Oct. 08 Sep. 11 Sep. 17 Sep. 24 Sep. 16 Sep. 25 Oct. 06 z denotes sites lost due to spring flooding.

3 GAUDET ET AL. * WINTER WHEAT SUSCEPTIBILITY TO COMMON BUNT 485 very susceptible to common bunt, whereas Blizzard, a cold-hardy winter wheat cultivar from the Pacific North-western USA, is highly resistant to bunt. Both non-inoculated and inoculated bunt treatments of the varieties were included in all test years. Plant vigour of the entire row was rated in May to obtain an indication of winter injury using a 1 to 4 scale based on survival and subsequent spring growth, where 1 poor survival/ low growth, and 4very good survival and spring recovery. Average daily soil temperatures, which represented the mean of the average day and night temperatures, were recorded at a 5-cm depth at established meteorological stations at test sites in Lethbridge and Saskatoon. Cultivar treatments within seeding dates were arranged in a split plot design with bunt inoculation serving as whole plots and varieties serving as subplots with four replicates. Each row was harvested at maturity and a minimum of 150 tillers per replicate were assessed to determine the percentage of tillers with a partially or fully bunted spike. The effects: year, cultivar, seeding date, bunt inoculation (Table 1), and all of the possible interactions among these main effects within locations were considered. ANOVA was conducted on the means were analysed for using the PROC GLM option using SAS software (SAS Institute, Inc., Cary, NC) and standard errors were calculated. Regression analysis was conducted by locations using soil temperatures as the independent variable and percentage bunt as the dependant variable. Test 2 was conducted to assess the level of bunt resistance in winter wheat varieties as part of the western Canadian Bunt Cooperative Registration Tests from 2004/2005 to 2010/2011 (Table 2). Entries in Table 2. Mean bunt levels for winter wheat varieties included in the Winter Wheat Bunt Cooperative Registration Tests seeded at Lethbridge from 2004/2005 to 2010/2011 Variety Number z Bunt (%) yx SE w Accipiter ABC 5.5 AC Bellatrix D 4.1 Broadview ABC 6.0 CDC Buteo A 4.4 CDC Falcon BC 3.9 CDC Harrier AB 4.0 CDC Osprey A 3.0 CDC Ptarmigan ABC 4.4 Radiant C 3.9 CDC Raptor AB 5.5 AC Tempest C 4.9 z Number denotes how many times the variety occurred as a single row plot in Co-op tests from 2004 to y Bunt (%) was visually estimated as percent bunted tillers. x ANOVA and least squares means generated using the SAS procedure Proc Mixed. w Standard error of the least squares means. AC Mean separation on adjusted means using TukeyKramer studentized range test. Means followed by the same letter are not significantly different at P0.05. these tests were inoculated with the composite of races (Gaudet and Puchalski 1989a) and planted at Lethbridge. The seeding dates for these tests were generally during the last week of September or the first week of October, depending on planting conditions. Plots consisted of 5-m-long rows, one row per cultivar, arranged in a modified augmented design with two replicates. The inoculum and inoculation techniques were as described above. At maturity, the percentage of tillers that were partially or full bunted per row was visually estimated. Analysis of variance was conducted using the PROC MIXED option using SAS software, where each site-year was considered a random variable. RESULTS AND DISCUSSION In Test 1, plots were discarded in both Saskatoon and Glenlea due to extensive mortality caused by spring flooding in 2008/2009 (Table 1). The main effects of year, cultivar, inoculation, seeding dates and all interactions between the main effects were significant (P ) for percentage bunt infection. Therefore, percentage bunt infection for dates within locations within years is shown individually in Figs. 1 to 3. Non-inoculated treatments were usually free of bunt, though occasionally bunt was observed at levels of less than 1% in the susceptible varieties CDC Osprey and Radiant (data not shown). The resistance in Blizzard was effective in all environments, with mean bunt levels within individual plots generally less than 1% but reaching as high 3% at Lethbridge in 2009 (Fig. 1). For the susceptible varieties Radiant and CDC Osprey, infection levels varied with seeding dates, location and years (P B0.001). Low average bunt levels were observed at Glenlea and Saskatoon during 2007/2008, whereas high average bunt levels were observed during the same year at Lethbridge. This suggested that poor infection conditions prevailed at these two sites in 2007/2008 compared with Lethbridge, despite the similarity in planting dates at all three locations in 2007 (Table 1). Later seeded treatments tended to exhibit higher infection levels compared with the earliest seeding dates. Under light infection conditions, bunt levels did not vary greatly among seeding dates (Figs. 13). However, the latest seeding dates were not always the most severely infected. For example, in 2009/2010 at both Glenlea and Lethbridge, seeded Oct. 08 and Oct. 06, respectively, infection levels were less severe than the two earlier seeding dates (Table 1, Figs. 1 and 2). Seeding dates before Sep. 01 (Table 1) in Lethbridge and before mid-september in Saskatoon and Glenlea were unfavourable for bunt infection. The earliest (Sep. 06) seeding date at Lethbridge in 2007/ 2008 exhibited infection levels of approximately 45%, which was similar to the later seeding dates during the same year. Overall, earlier seeding in Lethbridge in September still resulted in higher infection levels than correspondingly early seeding dates in both Saskatoon and Glenlea (Figs. 1 to 3).

4 486 CANADIAN JOURNAL OF PLANT SCIENCE Fig. 1. The effect of fall seeding date on percent bunt infection in three varieties of winter wheat during three growing seasons in Lethbridge, Alberta. BzdBlizzard, OspOsprey, Rad Radiant. Seeding into cool soils is known to increase the severity of common bunt (Holton and Heald 1941). Common bunt fungi have relatively low optimal temperatures for spore germination and infection, and these conditions are generally met by early seeding of spring wheat and late seeding of winter wheat (Holton and Heald 1941; Gaudet and Puchalski 1990). Teliospore germination of the bunt fungus coincides with germination of the wheat seedling shortly after seeding. Spore germination generally occurs 4 to 10 d after seeding (Lowther 1950; Russell and Mills 1994) and penetration of emerging wheat coleoptiles occurs 7 to 10 d after seeding of infested seed (Woolman 1930; Swinburne 1963). A successful infection results when the fungus grows through the coleoptile and several embryonic leaves to establish itself in the region directly below the apical meristem of the developing seedling before extension of the internodes during culm formation, a process, which takes place 3 to 5 wk after seeding Fig. 2. The effect of fall seeding date on percent bunt infection in three cultivars of winter wheat during two growing seasons in Glenlea, Manitoba. BzdBlizzard, OspOsprey, Rad Radiant. (Swinburne 1963; Fernandez et al. 1978). Environmental conditions, such as low average soil temperatures, that favour development of the pathogen and hinder plant development can increase the level of successful bunt infection. Mean soil temperatures at 5 cm depth, averaged over 45 d following seeding of CDC Osprey and Radiant at Lethbridge and Saskatoon, were negatively associated with infection levels (r , P 0.001) (Fig. 4) and positively associated with fall vigour (r , P0.001) (data not shown). Location effects for bunt infection levels between Lethbridge and Saskatoon were clearly evident. Based on regression statistics, Lethbridge was deemed more conducive for bunt infection compared with Saskatoon (P 0.001) despite the similarity of average soil temperatures in both locations (Fig. 4). Therefore, factors other than soil temperatures such as soil moisture and soil type likely account for the differences in infection observed between the two sites (Leukel 1937). The consistently high infection levels observed in the present study support empirical observations that Lethbridge is a preferred site for routine bunt screening of winter wheat. Significant main effects for variety, seeding date and years, and their interactions (P B0.05) were observed at all three locations for spring vigour. The earliest seeded

5 GAUDET ET AL. * WINTER WHEAT SUSCEPTIBILITY TO COMMON BUNT 487 Fig. 3. The effecting of fall seeding date on percent bunt infection in three varieties of winter wheat during three seasons in Saskatoon, Saskatchewan. BzdBlizzard, OspOsprey, RadRadiant. treatments tended to be the most vigorous in spring; the latest seeded treatments were the least vigorous (data not shown). These results are consistent with the need for sufficient plant development in the fall to permit Fig. 4. Association between autumn soil temperatures measured at 5 cm depth for 45 d after seeding with the incidence of common bunt during 2007/2008, 2008/2009 and 2009/2010 in Lethbridge, Alberta and during 2007/2008 and 2009/2010 in Saskatoon, Saskatchewan. maximum development of winter hardiness in western Canada (Fowler 1982, 2012). Winterkill was not evident in any of the treatments suggesting that the three varieties were sufficiently hardy to survive the prevailing winter conditions. Infection of the varieties with common bunt did not have any obvious negative effects on spring vigour ratings compared with the corresponding non-inoculated treatments at any of the locations during the 3 yr of this study. Veisz et al. (2000) reported that low temperature winterkill increased following bunt inoculation under controlled environment conditions. Failure to observe a similar tendency for winterkill in the present study may due to the lack of low temperature stress during the three winters of this study. In Test 2, all of the 11 western Canadian winter wheat varieties tested were susceptible to common bunt except AC Bellatrix (Table 2) (Thomas et al. 2012b). The source of the resistance in AC Bellatrix is unknown, although based on its pedigree (Turkey Red/Burt// Bezostaya 1 IDO180)*2/(Cheyenne/Kharkov 22MC Sundance), it could possess Bt1 and/or Bt4 originating from Burt (Kendrick and Holton 1961) and/or Bt7, which originates from Burt and Cheyenne (Martynov et al. 2004). However, races that overcome these three genes are common in North America (Hoffmann and Metzger 1976; Gaudet and Puchalski 1989b) and were included in the race composite in this study. For example, race L-16 possesses the virulence/avirulence formula 1,2,4,6,7/3,5,8,9,10, which will overcome any line that possesses any combination of Bt1, Bt4, and Bt7 (Hoffmann and Metzger 1976; Gaudet and Puchalski 1989b). It is possible that useful residual resistance is being provided by the presence or interaction of two or more of these defeated genes. Numerous examples of this phenomenon have been reported in the literature for various plant pathogens (Pedersen 1988). Additionally, Sundance has been shown to exhibit some resistance to common bunt (Grant 1972; Gaudet et al. 1994) suggesting that it may have contributed to the AC Bellatrix resistance. Also observed was variation in the level of susceptibility among winter wheat varieties; for example, Radiant and AC Tempest (Thomas and Graf 2012) were less susceptible than CDC Buteo (Fowler 2010), CDC Osprey and CDC Harrier (Fowler 1999) (Table 2). In contrast to the possible interaction of defeated genes resulting in the stable resistance expressed by AC Bellatrix, wheat genetic backgrounds that are highly susceptible to common bunt are likely to influence the level of expression of effective resistance genes (Gaudet et al. 1995) For example, Flourish winter wheat, registered in 2011 with good adaptation to the eastern prairie and parkland regions, only expresses moderate bunt resistance derived from the highly resistant variety Blizzard (Graf et al. 2012). In light of the results of these studies, the risk of common bunt infection to winter wheat production in western Canada remains high. Additionally, because low levels of infection produce downgrading of wheat

6 488 CANADIAN JOURNAL OF PLANT SCIENCE [0.05% by weight (Bailey et al. 2003)], the economic risk is even greater. Currently, the most important factor mitigating the risk of common bunt in wheat in western Canada is the lack of inoculum. The widespread resistance among varieties belonging to the most important wheat types, the CWRS and Canada Western Amber Durum classes (Gaudet and Puchalski 1989a), has resulted in a very low spore load for bunt in western Canada. In southern Alberta, the drier and milder conditions permit and often result in late September or early October seeding dates. The high infection levels associated with late seeding, particularly with highly susceptible winter wheat varieties will result in an elevated risk of bunt in this region if inoculum is permitted to build. To keep inoculum levels low, treating seed with effective fungicides is essential (Gaudet et al. 1989, 1994), as outbreaks of common bunt occur in this region when fungicides are not employed routinely (Gaudet, unpublished results). For the Parkland regions of Saskatchewan and Manitoba, planting of winter wheat by the first week of September is recommended to ensure good winter survival (Fowler 1982, 2012). Under these conditions, much of the seedling development will occur in warmer soils that are not conducive for infection by common bunt (Holton and Heald 1941). However, in some cases, later seeding may be unavoidable due to late maturity of the previous spring crop or adverse autumn weather conditions. Additionally, delaying seeding can reduce the risk of diseases such as stripe rust and wheat streak mosaic virus by eliminating the green bridge of infected plant material. Our results also demonstrated a location effect on bunt risk whereby lower infection levels, possibly due to different soil type, were observed at Saskatoon compared with Lethbridge despite similar soil temperatures during infection. These results suggest a lower risk for common bunt in Saskatchewan and Manitoba than for southern Alberta; however, a localized outbreak of common bunt occurred in winter wheat in Manitoba during This demonstrated that this disease may occur in these regions with current agronomic practices, despite generally low soil-borne inoculum levels. Coupled with the high susceptibility of currently available winter wheat varieties to common bunt, the need for routine seed treatment with fungicides in Saskatchewan and Manitoba is clear. CONCLUSIONS The risk for common bunt infection of winter wheat over much of the western Canadian prairies is high, particularly when susceptible varieties are seeded into cool soils in late September or early October. Even in early-seeded treatments in the eastern prairies, high infection levels were possible. These results coupled with recent increases in the number of hectares seeded to winter wheat (Fowler 2012) and a general failure to treat seed with effective fungicides (Gaudet et al. 1989), reveal an impending threat of common bunt to winter wheat production in western Canada. In light of these results, we recommend judicious use of effective seed treatment fungicides until resistance to common bunt can be incorporated into new winter wheat varieties for western Canada. These measures will keep the spore load at very low levels and ensure the long-term stability of genetic resistance. Bailey, K. L., Gossen, B. D., Gugel, R. K. and Morrall, R. A. A Diseases of field crops in Canada. The Canadian Phytopathological Society and University Extension Press, University of Saskatchewan, Saskatoon, SK. Cherewick, W. J Smut diseases of cultivated plants in Canada. 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