Abstract
Commercial fields and research plots of wheat across Canada were surveyed for leaf rust during 2008. Leaf samples infected with the causal fungus, Puccinia triticina, were used to generate 407 single pustule isolates, 13 from Alberta, 302 from Manitoba and Saskatchewan, 71 from Ontario, 10 from Quebec and 11 from Prince Edward Island. Single pustule isolates were tested for virulence to 16 lines of ‘Thatcher’ wheat with single leaf rust resistance genes. Forty-six virulence phenotypes were identified; the most common were TDBJ (23.6%), TDBG (23.1%) and MLDS (18.9%). The frequency of virulence to both Lr9 and Lr17 increased compared with 2007, whereas it decreased for Lr24 and Lr2a. The populations from eastern Canada were more diverse than those from western Canada and contained many unique virulence phenotypes, and virulence to gene Lr18, which was not found in western Canada. Fifty-five isolates, representing each of the virulence phenotypes, were tested on six and 12 additional differential wheat lines at the adult and seedling stages, respectively. On the adult plant differentials, no isolates were virulent to Lr22a or Lr34, whereas all isolates except two were virulent to Lr13, and virulence varied for Lr12, Lr35 and Lr37. On the additional seedling differentials, all isolates were avirulent to Lr19, Lr21, Lr29 and Lr32, and only one isolate was virulent to Lr25. All isolates had similar infection types to Lr2b and Lr2a, varied in virulence to Lr3bg, Lr14b, Lr20, Lr23 and Lr28, and except for two were virulent to Lr15.
Résumé
Au Canada, en 2008, les champs de blé et les parcelles expérimentales ont été inspectés afin d'y déceler la rouille des feuilles. Des échantillons de feuilles infectées par l'agent causal Puccinia triticina ont été utilisés pour produire 407 isolats à partir de pustules individuelles, dont 13 de l'Alberta, 302 du Manitoba et de la Saskatchewan, 71 de l'Ontario, 10 du Québec et 11 de l’Île-du-Prince-Édouard. Des isolats issus de ces pustules ont été testés quant à la virulence à l’égard de 16 lignées de blé ‘Thatcher’ possédant un gène unique de résistance à la rouille des feuilles. Quarante-six phénotypes de virulences ont été identifiés, les plus courants étant TDBJ (23,6 %), TDBG (23,1 %) et MLDS (18,9 %). La fréquence de virulence à l’égard des gènes Lr9 et Lr17 a augmenté comparativement à 2007, tandis qu'elle a décru par rapport à Lr24 et Lr2a. Les populations de l'Est canadien étaient plus diversifiées que celles de l'Ouest canadien et possédaient de nombreux phénotypes uniques de virulence. De plus, la virulence à l’égard du gène Lr18 n'a pas été détectée dans l'Ouest. Cinquante-cinq isolats, représentant tous les phénotypes de virulence, ont été testés sur 6 et 12 lignées différentielles additionnelles de blé aux stades adulte et semis, respectivement. En ce qui a trait aux lignées au stade adulte, aucun isolat n’était virulent à l’égard des gènes Lr22a ou Lr34, tandis que tous, sauf deux, l’étaient à l’égard de Lr13. Par ailleurs, la virulence variait à l’égard des gènes Lr12, Lr35 et Lr37. Quant aux lignées au stade semis, tous les isolats étaient non virulents à l’égard de Lr19, Lr21, Lr29 et Lr32. Un isolat seulement était virulent à l’égard du gène Lr25. Tous ont affiché des types similaires d'infection à l’égard de Lr2b et de Lr2a, une virulence variable à l’égard de Lr3bg, Lr14b, Lr20, Lr23 ainsi que de Lr28 et, à l'exception de deux, tous étaient virulents à l’égard du gène Lr15.
Introduction
There were approximately 10.2 M ha seeded to wheat in Canada during 2008, including 7.0 M ha of hexaploid spring wheat (Triticum aestivum L.), 2.2 M ha of durum wheat (Triticum turgidum L. ssp. durum (Desf.) Husn.) and 0.9 M ha of winter wheat (T. aestivum) (Statistics Canada, Citation2011). Canada western red spring (CWRS) wheat class accounted for approximately 5.3 M ha of the hexaploid spring wheat area planted, with other wheat classes accounting for the remaining seeded area. The most commonly grown CWRS cultivars in 2008 were ‘Lillian’, ‘Harvest’, and ‘Superb’, grown on 16.4%, 13.2% and 11.5%, respectively, of the total area seeded to CWRS cultivars (Anonymous, Citation2009). The leaf rust resistance genes in ‘Lillian’ and ‘Harvest’ are not known, although it appears that ‘Lillian’ has Lr30 and Lr34, along with other genes (B. McCallum, unpublished data). The cultivar ‘Superb’ was demonstrated to have Lr2a and Lr10 (McCallum & Seto-Goh, Citation2010). In inoculated field trials in 2008, ‘Lillian’ was resistant, ‘Harvest’ was moderately resistant and ‘Superb’ was susceptible. There was also 0.67 M ha seeded to wheat in eastern Canada, with winter wheat in Ontario accounting for 0.51 M ha and the rest primarily spring wheat in the other eastern provinces (Statistics Canada, Citation2011).
Wheat leaf rust, caused by Puccinia triticina Eriks. (Anikster et al., Citation1997) (= P. recondita Rob. ex Desmaz. f. sp. tritici), is a historic and current production problem on wheat in Canada and other parts of the world. The disease reduces yield by 5–25%, depending on the susceptibility of the crop, fungicide application and the timing of infection (McCallum et al., Citation2007). Virulence surveys have been conducted annually in Canada since 1931 to monitor changes in the P. triticina population. These surveys can detect new virulence phenotypes, provide a historic record of shifts in virulence to specific resistance genes, and detect groups of genetically similar isolates (Wang et al., Citation2010). Knowledge on the virulence of the P. triticina population and the resistance genes in Canadian wheat cultivars can be used to make informed decisions on breeding and developing new wheat cultivars with effective resistance (McCallum and DePauw, Citation2008).
The main objective of this study was to determine the frequency and distribution of virulence phenotypes from P. triticina isolates collected across Canada, using 16 near-isogenic wheat lines inoculated at the seedling stage, each carrying a different gene for seedling leaf rust resistance. A second objective was to determine the virulence spectrum for representative isolates of all the virulence phenotypes found in 2008, on six additional near-isogenic wheat lines with adult plant resistance genes and 12 additional near-isogenic lines with seedling resistance.
Materials and methods
Infected wheat leaves were collected from individual fields and nurseries from June–September in 2008 at various locations throughout Prince Edward Island (PEI), Ontario, Quebec, Manitoba, Saskatchewan and Alberta. The leaves were air dried at 20–27 °C for approximately 12 to 24 h then stored separately for 2–4 mo at 5 °C. Puccinia triticina urediniospores from individual collections were subsequently scraped off from infected leaves using a metal spatula and a small amount of water, and inoculated onto the susceptible wheat cultivar ‘Little Club’ by rubbing the leaves with a urediniospore, water and Tween 20 mixture as described previously (McCallum & Seto-Goh, Citation2005). Each pot containing ‘Little Club’ seedlings was pretreated with 50 mL maleic hydrazide solution (0.36 g L−1) approximately 5 d after seeding to prevent the emergence of secondary leaves and to produce larger uredinia with abundant sporulation. A plastic cone, approximately 25 cm in height, with an open top was placed over each pot to minimize cross contamination. Inoculated plants were placed into a dew chamber (Model I-60D, Percival Scientific, Perry, IA) with nearly 100% relative humidity for approximately 17 h to allow the urediniospores to germinate and initiate the infection process, then placed into a greenhouse at 20 ± 4 °C with supplemental high-pressure sodium lighting. Approximately 7 d after inoculation, chlorotic spots appeared, indicating areas of infection. The leaves were then trimmed so that single isolated uredinia remained on the upper edge of each trimmed leaf. Other plants and leaves were removed so only three to four plants with isolated uredinia remained. At approximately 14 d after inoculation, urediniospores were collected from a single isolated uredinium into a 00 gelatin capsule, using a vacuum suction micro-collector, mixed with a light mineral oil (Bayol, Esso Canada, Toronto, ON) and sprayed onto a 7-d-old set of wheat seedlings which included ‘Thatcher’ and 16 single resistance gene ‘Thatcher’ near-isogenic lines. Two single uredinial isolates were typically evaluated from each rust collection, although sometimes one or three isolates per collection were analysed. Approximately 12 seeds of each ‘Thatcher’ near-isogenic line were planted in a clump and the clumps were evenly spaced in a fibre flat (25 × 15 cm). Plants were pretreated with maleic hydrazide as described above. Previous experiments demonstrated that pretreatment with maleic hydrazide does not alter the virulence determination but results in shorter greener leaves which clarify the pustule phenotype (B. McCallum, unpublished results). After inoculation, the plants were dried for at least 1 h to allow the oil to evaporate and then incubated and maintained as described above. Infection types produced on the 12 standardized differentials [Set 1: Lr1 (RL6003a), Lr2a (RL6016), Lr2c (RL6047), Lr3 (RL6002); Set 2: Lr9 (RL6010), Lr16 (RL6005), Lr24 (RL6064), Lr26 (RL6078); Set 3: Lr3ka (RL6007), Lr11 (RL6053), Lr17 (RL6008), Lr30 (RL6049)] were used to determine the three-letter code according to the virulence phenotype nomenclature (Long & Kolmer, Citation1989). Four supplemental differentials [Set 4: LrB (RL6051), Lr10 (RL6004), Lr14a (RL6013), Lr18 (RL6009)] were added to provide additional virulence information about the isolates, resulting in a four-letter code. All isolates were also inoculated onto ‘Thatcher’ and Lr1 + LrCen (RL6003b). The resistance gene temporarily named LrCen was previously identified in the Thatcher-Lr1 near-isogenic line RL6003 (McCallum & Seto-Goh, Citation2006 b; McCallum et al., Citation2006). Infection types to all the differential near-isogenic lines were rated 12 d after inoculation. Isolates that produced infection types ‘;’ (hypersensitive flecks), ‘1’ (small uredinia with necrosis), and ‘2’ (small to medium sized uredinia with chlorosis) were considered avirulent and those that produced infection types ‘3’ (medium sized uredinia without chlorosis or necrosis) and ‘4’ (large uredinia without chlorosis or necrosis) were considered virulent (Long & Kolmer, Citation1989). Inoculations were repeated if the infection response was not clear.
Fifty-five isolates which included at least one from most of the virulence phenotypes identified were inoculated onto adult plants of ‘Thatcher’ and six ‘Thatcher’ near-isogenic lines (Lr12 [RL6011], Lr13 [RL4031], Lr34 [RL6091], Lr22a [RL6044], Lr35 [RL6082], or Lr37 [RL6081]). Single plants of four ‘Thatcher’ near-isogenic lines and ‘Thatcher’ were grown together in a 15-cm-diameter pot and the other two near-isogenic lines and ‘Thatcher’ were grown in a second pot in the greenhouse at day/night temperatures of 25/18 °C with supplemental high-pressure sodium lighting. Plants were trimmed so that only two or three culms per plant remained. Flag leaves of two to three culms from each of the plants within a pot were inoculated with a single pustule isolate. The inoculated plants were incubated overnight in a dew chamber and grown in the greenhouse as described previously. Infection types were evaluated 14 d after inoculation. This subset of isolates was also tested on 12 additional ‘Thatcher’ near-isogenic lines at the seedling stage (Lr2b [RL6019], Lr3bg [RL6042], Lr14b [RL6006], Lr15 [RL6052], Lr19 [RL6040], Lr20 [RL6092], Lr21 [RL6043], Lr23 [RL6012], Lr25 [RL6084], Lr28 [RL6079], Lr29 [RL6080] and Lr32 [RL6086]). These isolates were also retested on seedling plants of the set of 16 ‘Thatcher’ near-isogenic lines mentioned previously to confirm the reactions, since many of these resistance genes (particularly Lr18 and LrB) are sensitive to temperature and other conditions. Inoculation, incubation and rating were as described previously for seedling evaluation.
Results and discussion
Wheat leaf rust severity was relatively light in western Canada during 2008 (McCallum & Seto-Goh, Citation2009 a). These lower than average levels of infection could have been due to low inoculum levels coming into Canada from the United States (Kolmer et al., Citation2010), fungicide application which was common on wheat, and cool temperatures during the growing season which appeared to slow the epidemic development. In a survey of 31 wheat fields in southern Ontario, leaf rust was found in 23 fields at moderate disease levels (Xue et al., Citation2009).
There were 407 single pustule isolates analysed in 2008, 13 from Alberta, 302 from Manitoba and Saskatchewan, 71 from Ontario, 10 from Quebec and 11 from PEI. In total, there were 46 unique virulence phenotypes identified, only 10 of these were found in more than one region of the country. The most common virulence phenotypes in Canada were TDBJ (23.6%), TDBG (23.1%) and MLDS (18.9%) (). Each of these virulence phenotypes was also common in previous years (), although MLDS and TDBJ increased whereas TDBG decreased when compared with 2007. TDBJ and TDBG have both been commonly found since 2005 and differ when compared with TBBJ and TBBG for virulence to Lr24 ().
Table 1. Frequency and distribution of virulence phenotypes of Puccinia triticina in Canada in 2008 identified by infection types when inoculated onto 16 ‘Thatcher’ near-isogenic lines
Table 2. Frequency (%) of predominant P. triticina virulence phenotypes in Canada from 2000 to 2008
Nearly all isolates were virulent to Lr1, Lr3 and Lr10 whereas less than 10% of the isolates were virulent to Lr16, Lr11 and Lr18 (). The frequencies of virulence to Lr9, Lr24, Lr17 and Lr2a have changed fairly dramatically over the past few years (), whereas most others have remained relatively stable. The frequency of virulence to Lr9 increased from 2.8% in 2006, to 8.7% in 2007, and then 19.7% in 2008 (). In the years prior to 2006, virulence to Lr9 was very rare. Similarly, less than 10% of the isolates were virulent to Lr24 prior to 2005 but since that year, over 65% of the isolates were virulent to Lr24. Virulence to Lr17 increased from 23.1% of the isolates in 2007, to 47.4% of the isolates in 2008. However, the frequency of virulence to Lr2a declined from 75.1% in 2007 to 51.1% in 2008. Selection for virulence to Lr9, Lr24 and Lr17 was thought to be driven by wheat cultivars in the United States carrying these resistance genes (Kolmer et al., Citation2007). While Lr9 and Lr17 are not known to be present in Canadian wheat cultivars, Lr24 is likely present in the winter wheat cultivar ‘Vienna’ grown in eastern Canada (B. McCallum, unpublished). Therefore, some level of selection for virulence to Lr24 may also occur in Canada.
Figure 1. Frequency of virulence (%) from 2000–2007 in the Manitoba and Saskatchewan population of P. triticina to near-isogenic lines containing Lr2a, Lr14a, Lr16, Lr17 or Lr24. a
Table 3. Frequencies of virulence of Puccinia triticina in Canada in 2007 to lines of wheat with single Lr genes for leaf rust resistance
There were five virulence phenotypes identified among 13 isolates from Alberta. Of these TDBG and MLDS were the most common, each with four isolates (). The Alberta collection resembled the much larger collection from Manitoba and Saskatchewan as these phenotypes were most common in both regions. In previous years, the population in Alberta and British Columbia was similar to that in Manitoba and Saskatchewan, but also contained unique virulence phenotypes. In 2008, only TBBJ was unique to Alberta, although this virulence phenotype was common in other regions in previous years ().
There were 17 virulence phenotypes identified from 302 isolates collected in Manitoba and Saskatchewan (). The most common were TDBJ (29.8%), TDBG (29.1%) and MLDS (20.5%). These were also common in this region in 2007 and previous years (). There has recently been an increase in phenotype MLDS. For virulence on these differentials, a previously dominant phenotype MBDS differs from MLDS only by avirulence to Lr9. Virulence to Lr9 in this region was previously rare or unknown until 2006, when the frequency of virulence started to increase primarily because of the appearance of MLDS isolates. Resistance gene Lr9 is not known to be used in Canadian wheat cultivars but has been used in United States wheat cultivars (Kolmer et al., Citation2007).
There were 27 virulence phenotypes identified from 71 isolates collected in Ontario, making it a much more diverse population than found in Manitoba and Saskatchewan (). The most common virulence phenotypes were MFDS (28.2%), MLDS (8.5%), MDDS and MBTN (both at 7.0%). Of the 27 virulence phenotypes found in Ontario, 15 were unique to this region of Canada. Two isolates from Ontario were virulent to Lr18, whereas none of the isolates from the larger sample in Manitoba and Saskatchewan were virulent (). Although this gene is not widely used in Canada, the wheat cultivar ‘Minnedosa’, which has Lr18, was released in Canada in 2008. This resistance would not remain fully effective if Lr18 virulent isolates were to appear in western Canada.
There were six virulence phenotypes identified among 10 isolates from Quebec (). Five isolates were MLDS, while each of the other phenotypes MCDS, PBLR, TBRK, TDPJ, and TLGJ had a single isolate. Virulence phenotypes MCDS, PBLR, TDPJ and TLGJ were only found in Quebec.
From PEI, there were eight virulence phenotypes found among 11 isolates (). Three isolates were MHNQ and two were MFGJ. The P. triticina population was found to be very distinct from those found in the rest of Canada in 2006 and 2007 (McCallum and Seto-Goh, Citation2009 b; McCallum et al., Citation2010). This was also true in 2008 as phenotypes MBNQ, MHNQ and TCRK were only found in PEI and not in the rest of Canada. There were also three isolates virulent to Lr16, which was rare in the rest of the country. The frequency of virulence to Lr26 (72.7%) was also higher in PEI than in any other region in the country. PEI is geographically isolated from the other wheat-growing regions in eastern Canada and likely the source of the inoculum that initiates the epidemic is distinct.
Fifty-five isolates were selected to represent most of the virulence phenotypes found in each of the regions of Canada. None were virulent to Lr22a or Lr34, whereas all were virulent to Lr13 except two (266-2 MBGJ and 190-1 MFGJ). Virulence frequency varied for Lr12, Lr35 and Lr37, with 85.4%, 5.4% and 72.7% of the isolates virulent, respectively (). Only 47 of the 55 isolates tested are shown in , since isolates with the same reaction on all differentials as another isolate were removed. Virulence for Lr12 and Lr37 has been relatively high in recent years, but virulence to Lr35 was previously rare. In 2008, seven of the isolates tested were virulent to Lr35.
Table 4. Infection types of 47 representative isolates from Canada in 2008 tested on near isogenic lines of ‘Thatcher’ with adult-plant resistance genes and additional seedling resistance genes
When the 55 selected isolates were tested for virulence to 12 additional ‘Thatcher’ near-isogenic lines at the seedling stage, all isolates were avirulent to Lr19, Lr21, Lr29 and Lr32, whereas only one isolate was virulent to Lr25 (188-2 TDBG). All isolates were virulent to Lr15 except 8-1 MDNS and 188-1 TDBJ. All isolates had a similar reaction to Lr2b as they did to Lr2a. Isolates varied in their reaction to Lr3bg, Lr14b, Lr20, Lr23 and Lr28 with 69.1%, 92.5%, 76.3%, 41.8% and 54.5% virulent isolates, respectively ().
While the severity of wheat leaf rust was relatively low in Canada during 2008, there was considerable variation in the P. triticina population. Ten of the 46 virulence phenotypes identified were found in more than one region, indicating a broad distribution of these relatively common phenotypes. Thirty-six phenotypes were found in a single region, and while most of these were relatively rare, they indicate some degree of differentiation between the regions. The populations in eastern Canada had many of the same virulence phenotypes found in western Canada, but also had many phenotypes not found in the much larger sample from the west. When reviewing virulence survey results over the period 1997 to 2007, Wang et al. (Citation2010) found distinctions between the populations in eastern and western Canada, with some degree of overlap. Kolmer (Citation1991) reported similar results for an earlier time period. The regions within eastern Canada (Ontario, Quebec and PEI) were also fairly distinct from each other, with many virulence phenotypes unique to one region or the other. The wheat cultivars grown in eastern Canada include both winter and spring types and leaf rust resistance genes are not as commonly deployed as they are in western Canada. The western Canadian wheat cultivars tend to have intermediate to high levels of leaf rust resistance conditioned by various combinations of resistance genes, which may have the effect of reducing diversity due to host selection (McCallum et al., Citation2007). The eastern populations may also be more distinct and diverse due to different sources of inoculum in the USA and potential over-wintering of leaf rust in eastern Canada (Wang et al., 2010).
Acknowledgements
We thank André Comeau, Denise Orr and Richard Martin who sent samples for analysis and other cooperators who grew trap rust nurseries.
Notes
Related Research Data
References
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