Evidence that wheat cultivars differ in their ability to build up inoculum of the takeall fungus, gaeumannomyces graminis var. tritici, under a first wheat crop

Evidence that wheat cultivars differ in their ability to buildup inoculum of the take-all fungus, Gaeumannomycesgraminis var. tritici, under a first wheat crop V. E. McMillan, K. E. Hammond-Kosack and R. J. Gutteridge* Department of Plant Pathology and Microbiology, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK The effect of wheat cultivar on the build-up of take-all inoculum during a first wheat crop was measured after harvest usinga soil core bioassay in field experiments over five growing seasons (2003–2008). Cultivar differences in individual years wereexplored by analysis of variance and a cross-season Residual Maximum Likelihood (REML) variance components analysiswas used to compare differences in those cultivars present in all years. Differences between cultivars in the build-up of inocu-lum were close to or at significance in two of the five trial years (2004 P < 0Æ05; 2006 P < 0Æ07), and current commerciallylisted cultivars were represented at both extremes of the range. In 2007 and 2008, when environmental conditions were mostfavourable for inoculum build-up, differences were not significant (P < 0Æ3). In 2005 the presence of Phialophora spp. at thetrial site restricted the build-up of take-all inoculum under all cultivars. The cross season REML variance components analy-sis detected significant differences (range: 3Æ4–47Æ8% roots infected in the soil core bioassay; P < 0Æ01) between the nine cul-tivars present in all years (excluding 2005). This is the first evidence of relatively consistent differences between hexaploidwheat cultivars in their interactions with the take-all fungus, and this could give an indication of those cultivars that couldbe grown as a first wheat crop, in order to reduce the risk of damaging take-all in a second wheat crop. This phenomenonhas been named the take-all inoculum build-up (TAB) trait.
Keywords: hexaploid wheat genotypes, inoculum build-up, Phialophora spp., soil core bioassay, take-all disease,Triticum aestivum been widely reported in the UK and Europe, but in Aus- tralia the dry and hot environment is reported to restrict Take-all, caused by the soil-borne ascomycete fungus the development of TAD (Yarham, 1981). Although first Gaeumannomyces graminis var. tritici (Ggt) (Walker, wheat crops usually show very little evidence of disease, 1981), is a devastating root disease of wheat and a serious they can build up inoculum in the soil rapidly from small constraint on wheat productivity in the UK and world- founder populations so that severe disease can occur in a wide (Hornby et al., 1998). Typical take-all symptoms following wheat crop. In the UK and elsewhere in Europe, show as black necrotic lesions on the roots and, when a large proportion of second and subsequent wheat crops severe, can spread to the stem base causing blackening are at risk from significant damage where take-all inocu- (Skou, 1981). Hyphae spread through the roots and destroy the vascular tissue. If severe disease occurs, typi- After harvest of a susceptible crop, the take-all fungus cal above ground symptoms can develop and show as survives saprotrophically on the dead roots and stem stunted plants and whiteheads caused by the premature bases, and this forms the main source of inoculum for the ripening of the crop. This significantly reduces grain yield next susceptible crop (Cook, 2003). However, Ggt is a and quality, and losses of up to 60% have been reported relatively poor saprotrophic competitor so that survival of inoculum rapidly declines in the absence of a living If consecutive wheat crops are grown, take-all is usu- host such as cereal volunteers and other efficient carriers ally negligible in first wheats, most severe in years 2–4, of the take-all fungus (Shipton, 1981). Consequently, a and then decreases. The latter phenomenon is known as 1 year break from susceptible cereals is usually sufficient take-all decline (TAD) (Slope & Cox, 1964). TAD has to reduce inoculum levels to negligible amounts. There-fore, damaging take-all can largely be avoided by only growing one susceptible crop at a time in the crop rota-tion (Yarham, 1981). However, on most soils, and due to current economic conditions, there has been a trend to Wheat germplasm influence on take-all inoculum increase the proportion of susceptible hosts in wheat- cultivars (Norman and Avalon), when grown as a first based rotations as the intensity of cropping increases and wheat, differed in their ability to build up take-all inocu- non-cereal break crops become less profitable (Hornby lum in the soil (Widdowson et al., 1985). In recent years, et al., 1998; Cook, 2003). Attempts to control take-all first wheat field trials at Rothamsted, within the Wheat using chemical, biological and cultural methods have met with only limited success, and with wheat as the domi- www.wgin.org.uk), have been used to study a wider nant UK crop for the cereal industry, take-all remains one range of cultivars and their differences in nitrogen use of the most difficult and important diseases to control.
uptake and utilization efficiencies (Barraclough et al.
Predicting the risk of severe take-all has always been (2010). It is the take-all inoculum data from these experi- difficult as many agronomic and cultural practices, as ments that are reported in this paper.
well as climatic conditions, can have an impact on howthe disease develops. A soil core bioassay, which mea- sures the take-all infectivity of the soil, can give an indica-tion of the potential risk to a following crop (Hornby, 1981). Such bioassays are very labour intensive and not,therefore, a practical option for assessing risk to commer- Field trials, one in each of the harvest years from 2004 to cial crops. However, the bioassay can be useful to study 2008, were all sited on the Rothamsted farm, Hertford- the biology of the disease in experimental situations and shire, UK, on flinty clay loam soil of the Batcombe soil ser- the percentage of roots infected in the bioassay after a first ies. The experiments were set up as fully randomized wheat crop is well correlated with observed amounts of block designs; treatments included three replicates of a take-all in both the spring and summer in the following range of 20–32 wheat cultivars in factorial combination second wheat crop (Hornby et al., 1998; Gutteridge et al., with 2, 3 or 4 different nitrogen rates (Table 1) (except the first year where cultivars were randomized in three The take-all infectivity of the soil, measured using the blocks and N rates were arranged in four sub-blocks in soil core bioassay, is widely interpreted as a gauge of the each main block (Barraclough et al., 2010)). Host geno- level of take-all inoculum in the soil (Hornby, 1981).
types included current commercial and semi-modern cul- However, the infectivity of the soil could also be influ- tivars in the UK together with a smaller number of enced by the biological and chemical properties of the soil, which could suppress this disease (Hornby, 1983) or All of the trials were grown as first wheat crops (sown by the differing pathogenicity of Ggt isolates present in a after oats) and established in the autumn (including particular field (Lebreton et al., 2007). Recently, a molec- spring cultivars), as part of the WGIN programme inves- ular method (not currently available in the UK) has been tigating nitrogen use efficiency in European wheat culti- developed in Australia to measure the amount of take-all vars (Barraclough et al., 2010). Seed rates were mostly in DNA in soil samples from the field (Ophel-Keller et al., the range 300–350 seeds m)1 but were sometimes larger 2008). This method directly quantifies the amount due to poor performance in seed germination tests and of take-all inoculum in the soil independently of other late sowing of some plots (due to seed delivery). Growth factors which may influence infectivity. Both Gutteridge regulator, herbicides and fungicides were applied accord- et al. (2008) and Bithell et al. (2009) have since shown a ing to the standard practice of the Rothamsted Farm.
good relationship between the DNA test and the soil corebioassay, thus supporting the interpretation that take-all inoculum levels are detected using the bioassay method.
Research done in the early 1980s, using the soil core A soil core bioassay (Slope et al., 1979; Gutteridge et al., bioassay method, suggested that two hexaploid wheat 2008) was used to measure the infectivity of the soil after Table 1 Details of field experimentsa used to measure the take-all inoculum building ability of wheat cultivars over five field seasons from 2004 to 2008 aField experiments were done as part of the Wheat Genetic Improvement Network programme (http://www.wgin.org.uk) to study nitrogen useefficiency in wheat. Additional details on these field trials are given in Barraclough et al. (2010).
bExcept cv. Chablis sown on 02 ⁄ 03 ⁄ 2004; cv. Paragon sown on 12 ⁄ 02 ⁄ 2004; cv. Zyta sown on 05 ⁄ 12 ⁄ 2003.
Table 2 Sampling information for the yearly first wheat field experiments (VSNI). Significant effects were supposed when P £ 0Æ05.
from 2004 to 2008, in which wheat cultivars were assessed after harvest for A cross-season Residual Maximum Likelihood (REML) their take-all inoculum building ability using a soil core bioassay variance components analysis was conducted for the ninecultivars that were tested in four of the five trial years (excluding 2005). In 2005, the high incidence of Phialophora spp. (as confirmed by microscopic analysis) restricted take-all inoculum build-up. Therefore these results were excluded from further analysis.
The infectivity of the soil, measured using the soil corebioassay, revealed that the amount of take-all inoculum aSampling was as soon after harvest as possible, weather left after a first wheat crop varied depending on wheat cultivar grown (Table 3). In each experiment there wasconsiderable variation in the amount of inoculum harvest from selected cultivars in years 2004–2006 and detected between replicate plots of the same wheat culti- all cultivars in 2007 and 2008, at one nitrogen applica- var. This reflects the known inherent ‘patchiness’ of take- tion rate (Table 2). The 200 kg N ha)1 was chosen for all in the field and the difficulties of conducting field trials sampling because this is closest to commercial applica- to study the take-all fungus (Hornby, 1981). As a conse- tion rates. Five soil cores (5Æ5 cm diameter by 10 cm quence, only two out of 5 years of the WGIN field trials deep) were taken in a zig-zag transect across each plot.
sampled show significant differences or close to signifi- Cores were inverted into plastic drinking cups (11 cm tall cant differences between cultivars in their ability to build with four drainage holes drilled in the bottom) which up small populations of the take-all fungus during a first contained a basal layer of 50 cm3 damp sand. The top of wheat crop (2004, P < 0Æ05; 2006, P < 0Æ07; Table 3).
the inverted soil core was pressed to the sides of the cup.
Results from 2007 and 2008, when overall amounts of The soil was lightly watered and 10 wheat seeds (cv.
inoculum were highest, were not significant (P < 0Æ3). In Hereward (RAGT, Cambridge, UK)) placed on the sur- 2005, inoculum levels were particularly low for all culti- face (originally the bottom of the core). Seeds were cov- vars and any effect of cultivar on inoculum build-up was ered with a layer of horticultural grit, and pots highly non-significant (P < 0Æ7). In this bioassay year, the transferred to a controlled environment room for presence of two competing and weakly parasitic root col- 5 weeks (16 h day, 70% RH, day ⁄ night temperatures onizing fungi, Phialophora graminicola and Phialophora 15 ⁄ 10°C and watered twice weekly). After 5 weeks the sp. lobed hyphopodia was detected by microscopy in plants were removed and the roots washed out with moderate to high abundance in all samples.
water. The roots were assessed for take-all lesions in a The overall level of take-all inoculum, measured using white dish under water and the total numbers of plants the soil core bioassay, differed considerably between and roots, and the numbers of plants and roots infected years (Table 3). This is most probably the result of annual were recorded. The percentages of plants and roots differences in environmental conditions. The main period infected were calculated as a measure of the infectivity of of inoculum build-up in a first wheat is from about May through to harvest (Slope & Gutteridge, 1979). In gen-eral, high temperatures and low rainfall limit inoculumbuild-up; conversely more moderate temperatures and higher rainfall, creating warm and moist soils, are more Roots with typical black take-all lesions viewed by eye in favourable (Hornby et al., 1998). Conditions in 2007 a white dish under water were recorded as above. In 2005 (total rainfall in May to August, 359 mm; mean max tem- a large proportion of roots from the bioassay showed pale peratures in each of the 4 months 20°C or less; Table 4) brown or grey discoloration and there was a noticeable were close to ideal, and this probably explains why lack of typical black take-all lesions. These discoloured amounts of inoculum were larger in that year than any roots were viewed under a binocular microscope (·25 other. However, in the other 4 years higher temperatures objective, ·10 eyepiece) and swollen cells typical of Phi- and ⁄ or lower rainfall during at least some part of this crit- alophora graminicola (anamorph of G. cylindrosporus) ical period probably explain, to a large extent, the gener- were seen on the grey roots, and Phialophora sp. lobed ally smaller amounts of inoculum that were detected. In hyphopodia (probable anamorph of G. graminis var.
2005, and as already indicated above, the presence of graminis) on the pale brown roots (Hornby et al., 1998).
Phialophora spp. almost certainly inhibited the take-allfungus and contributed to the very limited developmentof inoculum in that year.
When a subset of wheat cultivars, which were sampled The percentage of roots infected were transformed to log- in all years, were analysed using a cross season REML its and compared by analysis of variance using GENSTAT variance components analysis, the results showed that Wheat germplasm influence on take-all inoculum Table 3 Incidence of infected roots in the soil core bioassay used to measure the take-all inoculum building ability of winter wheat cultivars grown as first wheat crops and measured after harvest in field experiments from 2004 to 2008 Logit % roots with take-all (back-transformed means) aHigh incidence of Phialophora spp.
bIn 2004 cv. Avalon was sown late and the emerging seedlings were dislodged by feeding birds (rooks, Corvus frugilegus). As aconsequence all the replicated plots established a very low overall plant density compared with other cultivars in the trial.
Table 4 Monthly rainfal (mm) and average maximum temperatures (°C) ranked as a low builder, Riband a medium builder and recorded at Rothamsted from May to August for the field seasons from Hereward at the high-building end of the scale. The dif- 2004 to 2008 (data from the electronic Rothamsted Archive; e-RA) ference in the percentage of roots infected in the soil corebioassay between Cadenza and Hereward was 44Æ4% over the 4 years, showing clearly the contrasting ability of these particular cultivars to build up take-all inoculum The amount of inoculum in the soil at the time of sowing a susceptible crop greatly influences the amount of pri- mary infection that occurs in that crop and so helps to determine final disease severity (Bailey & Gilligan, 1999). Much of the previous research on take-all inocu- lum has focused on the capability of other crops and grass weeds to maintain and carry over inoculum in a breakyear (Gutteridge et al., 2006), the survival of Ggt inocu- the infectivity of the soil under these cultivars was highly lum in the field post-harvest (Macnish & Dodman, 1973; significantly different (P < 0Æ01; Table 5). Consistent Bithell et al., 2009), and how the length of the intercrop differences between cultivars were evident, with Cadenza Table 5 Mean percentage of roots infected in the soil core bioassay for between the take-all fungus and environmental condi- nine winter wheat cultivars, grown as first wheat crops, sampled after tions, as well as the known difficulties in measuring take- harvest over 4 years of field experiments (2004, 2006, 2007 and 2008)a.
all inoculum in the field due to uneven distribution and REML variance components analysis was used to analyse differences patchiness (Hornby, 1981), relatively consistent differ- ences in the ability of wheat cultivars to build up take-allinoculum over the study period are reported here. This phenomenon has been named as the take-all inoculum The soil core bioassay measures the infectivity of the sampled soil. As described in the introduction, the degree of infectivity detected could potentially be due to a num- ber of interacting factors, including the Ggt inoculum present, the type of soil microbial community present and ⁄ or the soil chemical properties which had each built up over the previous cropping period. In a previous study, a DNA-based detection test for Ggt was compared with the soil core bioassay at a range of infectivity levels and from two soil types (Gutteridge et al., 2008). This com- parative study revealed that a good correlation existed between DNA content of Ggt and the infectivity of the soil in two field experiments (linear regression r = 0Æ77 and 0Æ79) with a moderate correlation in a third fieldexperiment (linear regression r = 0Æ56). In addition, a2005 excluded from analysis due to the presence of competitive recent field experiments in New Zealand have also shown a good relationship between the two methods (Bithellet al., 2009). Based on these earlier results it is concludedthat the soil core bioassay is predominantly measuring period and environmental conditions influence inoculum take-all inoculum build-up. However, it is acknowledged decline in the soil (Colbach et al., 1997; Gutteridge & that the soil microbial community and ⁄ or the soil Hornby, 2003). The results presented in this paper, how- chemistries present in the collected soil sample could also ever, suggest that there are potentially important differ- influence the soil sample’s infectivity in the subsequent ences between hexaploid wheats in their propensity to bioassay. Post-collection, the soil samples are kept at 4°C and in the dark. This could successfully preserve different The build-up of inoculum during a first wheat crop can- types of soil microbial communities and soil chemistries not be reliably simulated in pot or laboratory tests using field soil (R. Gutteridge, unpublished data). This makes Excluding 2005, when Phialophora spp. were present, investigating inoculum build-up reliant on field trials the results from the other 4 years suggest that opportuni- which are time consuming and vulnerable to variation in ties may exist within current wheat germplasm to manip- environmental conditions from year to year. Previous ulate levels of natural take-all inoculum in the soil during research has shown that the progression of take-all epi- a first wheat crop by appropriate choice of cultivar, and demics from build-up to TAD is significantly influenced so reduce the risk of damaging disease occurring in the by environmental conditions (Slope & Gutteridge, 1979; following, second, wheat crop. Limiting the build-up of Bailey et al., 2005; Pillinger et al., 2005; Ennaifar et al., inoculum during a first wheat crop could lead to more 2007). High soil moisture levels have been associated profitable second wheat crops and give farmers more with more severe take-all epidemics (Pillinger et al., freedom in choosing rotational cycles which contain a 2005). Conversely, delay in the onset of epidemics has higher proportion of wheat crops. Yield differences been linked to cold weather (Bailey & Gilligan, 1999) between first and second wheats are typically 1–1Æ5 ton- which restricts mycelial growth and could also increase nes ha)1 (HGCA recommended list; http://www.hgca.
the rate of inoculum decay. Clearly environmental condi- com), and much of the yield difference is also considered tions have a considerable influence on the build-up of to be directly attributable to the effect of take-all (Hornby take-all inoculum in the soil and the progress of take-all et al., 1998). When take-all is severe, yield differences can epidemics. In 2007 and 2008, when conditions were most be even greater, so there is scope for a significant improve- favourable for the build-up of inoculum, the effect of cul- ment in second wheat yields by minimising inoculum tivar was less significant. Environmental conditions that build-up in first wheats. The soil core bioassay method are particularly conducive to the build-up of inoculum used here is time consuming and labour intensive and so can also result in relatively high inoculum levels under is not suitable for commercial use. However, the newly even ‘low building’ cultivars. This reveals that favourable developed DNA method (Ophel-Keller et al., 2008) could environmental conditions can mask cultivar effects to provide a powerful tool for measuring inoculum build-up some extent. However, despite the complex relationship in the soil and disease risk which is quicker and more Wheat germplasm influence on take-all inoculum suitable for commercial application. One problem with disease management programmes under commercial the DNA test is that it could overestimate the potential disease risk by detecting non infective, dead Ggt DNA.
Further work is now required to investigate the signifi- However, Gutteridge et al. (2008) have previously shown cance of the finding reported here. A number of studies a good correlation between the amount of Ggt DNA have previously correlated the percentage of roots measured using the DNA test and disease in the following infected in the soil core bioassay with disease in the field second wheat crop, suggesting that the amount of non- in the following crop (Hornby et al., 1998; Gutteridge infective take-all DNA found in field soils is low. If the et al., 2008; Bithell et al., 2009). In further field trials correlation between the DNA level of take-all fungus in more information could be gained by measuring take-all the soil and disease severity in the following crop could be in second wheat crops after different first wheat cultivars.
confirmed in further locations ⁄ soils throughout the UK, It would then be possible to determine whether the differ- the DNA test could be commercially useful to assess the ences in inoculum build-up reported here could be of real risk of take-all in second wheat crops.
value to help minimize disease in the following crop.
The mechanism(s) underlying cultivar differences in Within the continuing WGIN project, wheat cultivar inoculum build-up reported here have not been estab- rotational studies have already commenced to explore lished. It is not known whether the ability of a wheat culti- whether particular combinations of first and second var to build-up inoculum as a first wheat crop is related to wheat cultivars maximize or minimize disease levels in its susceptibility to take-all infection; historically only very small differences have been found between hexa- Also, although there are a number of studies on inocu- ploid wheat genotypes and their susceptibility to take-all lum decline between harvest and sowing in relation to the in both field and pot tests (Scott, 1981; Freeman & Ward, length of the inter-crop period and environmental condi- 2004). Furthermore, first wheats can generate significant tions (Macnish & Dodman, 1973; Slope & Gutteridge, amounts of inoculum despite having few visible symp- 1979; Wong, 1984; Colbach et al., 1997; Gutteridge & toms on the roots. Any mechanism(s) influencing inocu- Hornby, 2003; Bithell et al., 2009), it is not known if the lum build-up are therefore not likely to be related to the conditions created or mechanisms involved in differential susceptibility of wheat cultivars to root infection by the inoculum build-up between wheat cultivars could result take-all fungus. As discussed above, it is possible that in changes to the rate of inoculum decline between har- wheat cultivars could influence the soil microbial com- vest and sowing. It is possible that such differences could munity, perhaps as a result of differences in root exu- influence the disease outcome in the second wheat crop.
dates, root senescence and ⁄ or differences in root Further research and field trials could also indicate architecture affecting soil physical structure, and thus whether it is possible to speed up take-all epidemics and influence take-all inoculum survival and build-up. The the natural build-up of suppressive soils in consecutive occurrence of take-all decline (TAD), attributed to wheat crops (take-all decline). TAD describes the reduc- changes in the soil microbial community, is already well tion in take-all disease in consecutive wheat crops after a documented (Weller et al., 2002) so it is known that take- peak of take-all is reached in the 2nd to 4th years (Slope all can be influenced by such changes in the soil.
& Cox, 1964). It is perhaps possible that by selecting a The genetic basis of this phenomenon is also not yet high building cultivar as a first wheat, peak levels of take- known. The germplasm tested in these experiments was, all disease could be established more quickly and the soil genetically, highly diverse. The UK bread wheat cv. Here- pushed into decline over fewer seasons so that farmers ward was consistently the highest take-all inoculum could benefit when their intention is to grow consecutive builder, although cvs Shamrock and Soissons were as, or more, effective in 2008. The consistently low building Although the genetic or mechanistic basis of this phe- cultivars included the UK spring wheat Cadenza and both nomenon is not yet known, the use of different cultivars modern and semi-modern UK winter wheats with good to manipulate inoculum levels in the soil could provide grain quality characteristics, namely Xi19, Mercia and farmers with a practical solution to reduce the risk of Riband. Xi19 is one of the highest yielding UK damaging take-all disease in second wheat crops.
bread wheats and is closely related to another of the con-sistently low building cultivars, Cadenza (Xi19 pedigree: seeds.co.uk). The Cadenza pedigree is also present in This research formed part of the core project of the Cordiale ((Reaper · Cadenza) · Malacca; http://www.
Wheat Genetic Improvement Network (WGIN) which is kws-uk.com), a low to medium building cultivar sampled supported by a commission from the Department for in three of the five WGIN trial years. Other low and Environment, Food and Rural Affairs (Defra, AR0709).
medium building cultivars such as Mercia and Riband We thank Rodger White for his excellent statistical have pedigrees unrelated to Cadenza, Cordiale and Xi19.
advice. Sanja Treskic is thanked for assisting with soil This suggests the existence of a range of genetically sample collection. Rothamsted Research receives grant- diverse germplasm conferring the low TAB trait, which aided support from the Biotechnology and Biological could be used in breeding programmes if further research Sciences Research Council (BBSRC). Vanessa McMillan demonstrates that it has potential value in take-all is funded by a BBSRC-CASE quota studentship awarded to Rothamsted and supported by the Home Grown Cere- frequencies and disease severity on wheat roots in the field.
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