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Resistance in winter wheat lines to deoxynivalenol applied into florets at flowering stage and tolerance to phytotoxic effects on yield
Article first published online: 9 JAN 2012
© 2012 The Authors. Plant Pathology © 2012 BSPP
Volume 61, Issue 5, pages 925–933, October 2012
How to Cite
Horevaj, P., Brown-Guedira, G. and Milus, E. A. (2012), Resistance in winter wheat lines to deoxynivalenol applied into florets at flowering stage and tolerance to phytotoxic effects on yield. Plant Pathology, 61: 925–933. doi: 10.1111/j.1365-3059.2011.02568.x
- Issue published online: 4 SEP 2012
- Article first published online: 9 JAN 2012
- Published online 9 January 2012
- Fusarium graminearum;
- winter wheat
In Europe and North America, deoxynivalenol (DON) is the most prevalent mycotoxin associated with wheat head blight caused by Fusarium graminearum and Fusarium culmorum. Because DON is toxic to plants and enhances the ability of the pathogen to spread within a spike, wheat lines with resistance to DON should be more resistant to head blight. Resistance to DON has been associated with resistance gene Fhb1 that confers resistance to spread within a spike. The objectives of this study were to determine if wheat lines resistant to head blight were also resistant to DON, if genes other than Fhb1 confer resistance to DON, and to identify lines able to fill grain in the presence of DON. Susceptible controls and diverse North American and European winter wheat lines with resistance to head blight were screened for molecular markers linked to known head blight resistance genes, and evaluated in a greenhouse for resistance to DON and relative yield after application of DON to spikes at flowering. Fhb1 appeared to have the unique ability to confer resistance to DON, as measured by the number of DON-bleached primary florets. However, this resistance did not protect plants from the phytotoxic effects of DON on kernel formation as measured by the relative yield of treated spikes. Furthermore, measuring the relative yield loss following DON application may be useful for identifying lines with tolerance to head blight.
Deoxynivalenol (DON) is the most common toxin produced by Fusarium graminearum sensu lato (teleomorph Gibberella zeae) and Fusarium culmorum in wheat affected by fusarium head blight (FHB) in Europe and North America (Scott, 1997; Bottalico & Perrone, 2002; Chandler et al., 2003; Rasmussen et al., 2003). Because of known DON toxicity to humans and animals, wheat cultivars with low or no DON are desirable for wheat growers, processors and consumers (Bai & Shaner, 2004). In addition to its effects on animals, DON also inhibits protein synthesis in plant ribosomes, causing chlorosis, necrosis and wilting in plants (Casale & Hart, 1988). Further research (Feinberg & McLaughlin, 1989) determined that DON binds to a single site on the 60S ribosomal subunit and inhibits peptidyltransferase activity, which is required for polypeptide elongation and termination. This in turn inhibits DNA synthesis, enzymatic activity and cell division, allowing a rapid increase of disease symptoms.
More evidence on the role of DON in plant disease was provided when DON-nonproducing mutants of F. graminearum were obtained by disruption of the TRI5 gene (Proctor et al., 1995). As a result of TRI5 gene disruption, spread of head blight within wheat spikes was significantly reduced in comparison with the parent strain or revertants of the TRI5 mutations (Desjardins et al., 1996). Although TRI5 gene disruption mutants were less able to spread in wheat spikes, their ability to cause initial infections was not reduced (Bai et al., 2001). Therefore, DON is not necessary for initial infection by the fungus, but it appears to act as an aggressiveness factor by enhancing the ability of F. graminearum to spread within a spike. Wheat lines with resistance to DON may therefore be more resistant to spread of the disease within spikes.
Miller et al. (1985) observed that certain head blight-resistant cultivars of wheat and rye inhibited DON synthesis and/or promoted degradation of DON, and this phenomenon was proposed as a new type of resistance (Miller & Arnison, 1986). Wang & Miller (1988) measured a decrease in growth of wheat coleoptile segments exposed to a range of DON concentrations. They observed a significant correlation between toxin resistance and head blight resistance in the field, and head blight-resistant cultivars were 10–100 times more tolerant of DON than susceptible cultivars. Shimada & Otani (1990) measured inhibitory effects of DON on the growth of wheat shoots and roots, and Bruins et al. (1993) measured the effects of DON on wheat coleoptiles, anther-derived callus and anther-derived embryos. Although DON inhibited growth of various types of wheat tissues in these studies, it can be concluded that even though DON is phytotoxic to plant tissues, sensitivity to DON among wheat lines is not consistently correlated with resistance to head blight. Nevertheless, as McCormick (2003) suggested, several factors such as stage of plant development (germination vs. flowering), type of tissue treated with DON (wheat roots vs. wheat spikes), and different procedures of toxin application (plating of kernels or floret parts on DON-amended media vs. direct application of DON into wheat spikes) can play a role in the association of resistance to DON with resistance to head blight.
Bushnell et al. (2010) investigated the effects of DON on content of chloroplast pigments in barley leaf tissues. Uninfected leaf segments of susceptible cv. Robust with exposed mesophyll cells were floated on DON solutions in dark or in light. They concluded that the loss of chlorophyll (bleaching symptoms) was light dependent and a secondary effect of DON, not required for toxicity. The primary effect of DON was damage to the plasmalemma, and this was demonstrated by the loss of electrolytes even in the dark, although the tissues remained green.
Lemmens et al. (2005) applied DON directly into wheat spikes of doubled haploid lines originating from the cross of head blight-resistant CM-82036 and head blight-susceptible Remus and counted the number of bleached florets after application. They found that resistance to DON was closely associated with an important head blight resistance gene, Qfhs.ndsu-3BS (now known as Fhb1). Furthermore, in wheat lines with Fhb1, the applied toxin was converted to DON-3-O-glucoside which appears to have low or no toxicity to plants (Engelhardt et al., 1999; Poppenberger et al., 2003). Lemmens et al. (2005) hypothesized that Fhb1, which was previously identified as conferring resistance to spread of symptoms in the spike, encodes for or regulates the expression of a DON-glucosyl-transferase enzyme that converts DON to DON-3-O-glucoside and thereby slows the spread of head blight symptoms in wheat spikes. Although DON-3-O-glucoside appears to have low or no toxicity to plants, its effects on animal systems are largely unknown. Glucosidated forms of mycotoxins are not detected during routine mycotoxin analyses; however, these glucosidated compounds are probably hydrolysed to the original mycotoxin during digestion in animals (Gareis et al., 1990; Berthiller et al., 2005). Because glucosidated mycotoxins escape detection but probably have ill effects on animals, they have been called ‘masked mycotoxins’. DON-3-O-glucoside has been reported as a masked mycotoxin in wheat (Berthiller et al., 2005), maize (Berthiller et al., 2009) and beer and some brewing intermediates (Kostelanska et al., 2009).
Kernels from apical portions of head blight-diseased spikes may be reduced in size and density as a result of vascular blocking by the pathogen even though these kernels are not colonized by F. graminearum (Bai & Shaner, 1994). This phenomenon may be an important component of yield and test weight losses in the field. Mesterházy (1995) reported variation among cultivars for yield reduction at a given level of head blight severity and proposed this phenomenon as a separate type of resistance called tolerance against head blight. Also, Rudd et al. (2001) suggested that from a practical breeding perspective, the measurement of grain yield under heavy disease pressure (tolerance) could be a valuable tool for combining both grain yield and head blight resistance as breeding objectives. Atanassov et al. (1994) inoculated seven wheat lines of different resistance levels with six strains of three Fusarium species. Reductions in grain weight were positively correlated with mycotoxin concentrations, and these correlation coefficients were higher for the more aggressive strains. These results support the importance of DON for disease development and yield. Bushnell et al. (2003) suggested that early and rapid filling of grain could be factors conferring tolerance; however, they noted that establishing tolerance as a separate resistance component can be complicated due to difficulties of accurate disease assessment over prolonged periods of disease development.
The objectives of this study were: (i) to determine if wheat lines resistant to head blight were also resistant to DON; (ii) to determine if genes other than Fhb1 confer resistance to DON; and (iii) to identify lines able to fill grain in the presence of DON.
Materials and methods
The effects of DON on blighting and relative yield of wheat lines were investigated in two similar experiments. Experiment 1 included one susceptible line and 15 diverse wheat lines (Table 1) with both type I (resistance to initial infection) and type II (resistance to spread within a spike) resistances to head blight (Horevaj et al., 2011). Experiment 2 included three susceptible and eight head blight-resistant lines of European origin (Table 1). The head blight resistance was based on reactions in field tests (Buerstmayr et al., 2008; Holzapfel et al., 2008; Veskrna et al., 2009), but the type of resistance was not classified. To produce adult plants for both experiments, seeds were germinated for 72 h on germination paper at room temperature. The most vigorous seedlings were transplanted into 7·5 cm pots (five seedlings per pot) containing potting mix (six parts peat moss, four parts vermiculite, two parts perlite, three parts Roxana silt loam soil, and three parts sand). Plants were vernalized for 8–9 weeks in a growth chamber programmed from 08·00 to 20·00 h at 8°C and from 20·00 to 08·00 h at 5°C with a 12 h photoperiod. After vernalization, plants were transplanted into 15 cm pots and moved to a greenhouse at 17–22°C and with a 14 h photoperiod. Each pot was fertilized with 6 g of Osmocote 14-14-14 (N-P-K) slow release fertilizer (The Scotts Company LLC) and 34 mg of Soluble Trace Element Mix (The Scotts Company LLC). After vernalization, plants were treated every 3 weeks with imidacloprid insecticide (Marathon; OHP, Inc.) at the rate of 5 mg a.i. per pot to control aphids, thrips and Barley yellow dwarf virus.
|VA04W-433||1||Ning7840/Pio2684//VA96-54-244 (CK9803/Freedom)||+||1 + ,4−||−||−|
|Fg 368||1||Zugoly/Reka/Nobeoka Bozu||+*||−||−||−|
|SZ 13||1||Ringo Star/Nobeoka Bozu||+*||−||−||−|
|SZ 14||1||Ringo Star/Nobeoka Bozu||+*||−||−||2 + ,3−|
|ARGE97-1047-4-2||1||Pio2684/3 Ning7840/Parula/Veery # 6||2 + ,3−||−||−||−|
|ARGE97-1033-10-2||1||Freedom/Catbird||−||2 + ,3−||−||−|
|AR97002-2-1||1||AR396-4-2/Ning8026||−||1 + ,4−||−||4 + ,1−|
|Fg 365||1||Ságvári/Nobeoka Bozu/Mini Mano/Sum3||−||−||−||−|
|Coker 9835||1||Susceptible control||−||−||−||−|
|Apache||2||Axial/NRPB-84-4233 (2530); (DER) Axial (Uslovno)||−||−||−||−|
|Rheia||2||Hubertus/SG-U-153-A (1336) (2810) (3035)||−||−||−||−|
Genotyping of wheat lines
To determine the likely presence or absence of FHB resistance genes and QTL, five plants of each line were genotyped at the USDA, ARS Eastern Regional Small Grains Genotyping Laboratory using linked molecular markers that were believed to be useful for identifying resistance genes in wheat lines that were not related to the mapping populations in which the markers were discovered. After vernalization, approximately 25 mg of leaf tissue was collected from each of five seedlings per line, stored in 1·1 mL microtubes with silica gel, and sent to the genotyping laboratory. Tissue was macerated using steel beads with a GenoGrinder 2000 (SPEX CertiPrep®), and extractions were performed according to the protocol of Pallotta et al. (2003). The PCR master mix consisted of 2 μL of 20 ng μL−1 genomic DNA template, 0·40 μL of a 10 μm mixture of forward and reverse primers, 0·18 μL (0·9 U) of Taq DNA polymerase, 1·20 μL of 10 × buffer (10 mm Tris-HCl, 50 mm KCl, 1·5 mm MgCl2, pH 8·3), 0·96 μL of a 100 μm mixture of dNTPs, and 7·26 μL of water, bringing the total reaction volume to 12 μL. A touchdown profile was used that consisted of an initial denaturation at 95°C followed by 15 cycles of 95°C (45 s), 65°C (45 s) decreasing by 1°C each cycle, and 72°C (60 s), followed by 25 cycles of 50°C annealing temperature. The forward primers were 5′-modified to include the fluorescent dye 6-FAM. Amplifications were performed using an Eppendorf Mastercycler® (Eppendorf AG). Sizing of PCR products was performed by capillary electrophoresis using an ABI3130xl Genetic Analyzer (Applied BioSystems). Analysis of PCR fragments was performed using GeneMarker 1·60 software (SoftGenetics). Markers for the resistance genes and QTL were as follows: Fhb1 = UMN10 (Liu et al., 2008) and gwm533 (Pumphrey et al., 2007); Fhb3 = cfd233 (Guyomarc’h et al., 2002) and gwm539 (Somers et al., 2003); 3BSc QTL = gwm285 (Somers et al., 2003), wmc1, wmc307, wmc418 and wmc612 (Somers & Isaac, 2004); and 5AS QTL = gwm304 (Somers et al., 2004) and wmc705 (Somers & Isaac, 2004).
DON application into spikes, visual evaluation of symptoms, and relative yield
To determine the levels of resistance and tolerance to DON, two pairs of similar-sized spikes in the early flowering stage (with protruding anthers in the centre of the spike) were selected in each pot and marked on the peduncle using a black non-toxic permanent pen (Sharpie). One spike of each pair served as a control, and the other spike was treated with DON using a modification of the procedure described by Lemmens et al. (2005). In wheat, each spikelet usually has two primary florets that are largest and first to flower (Allan, 1980). Ten microlitres of DON solution (25 μg μL−1 in 0·1% Tween 20) were applied into the four primary florets of two adjacent spikelets near the middle of the spike, resulting in the application of 1 mg of DON per spike. The four comparable florets of control spikes were treated with 10 μL of 0·1% Tween 20. Treated florets were marked by clipping of a small part of the tips of the glumes with scissors. To achieve high humidity needed for DON uptake, the pair of spikes was bagged together in a plastic bag for 48 h. The storage, handling and application of DON were done according to University of Arkansas Institutional Biosafety Committee Protocol # 07017.
In Experiment 1, the experimental design was a completely randomized design consisting of 16 wheat lines and five replications (pots) in run 1 and four replications in runs 2 and 3. In Experiment 2, the experimental design was a completely randomized design consisting of 11 wheat lines and five replications (pots) in runs 1 and 2. The total number of primary florets per spike was counted 7 days after treatment. At 7, 14 and 21 days after treatment, the number of bleached florets was counted. Spikes were harvested at maturity and threshed by hand to retain all grain. The relative yield for the treated spikes was calculated as yield for treated spikes divided by yield for control spikes multiplied by 100. Pearson correlation analyses were done to determine if resistance to DON, as measured by the number of DON-bleached primary florets, was associated with the total number of primary florets per spike. Data for the two treated and two control spikes within each pot were averaged prior to statistical analysis. Data were analysed using Proc GLM, sas version 9·1·3 (SAS Institute). Lines were treated as fixed effects and runs and replications as random effects. Means were separated using Tukey’s HSD test at P = 0·05.
Markers for resistance genes and QTL
Of the 27 wheat lines in Experiments 1 and 2, VA04W-433 and NC03-11465 appeared to be homozygous and homogeneous for both molecular markers linked to Fhb1, lines Fg 368, SZ 13 and SZ 14 had four plants homozygous and one plant heterozygous for both markers, and ARGE97-1047-4-2 was heterogeneous for the markers (markers were present only in two of five tested plants, indicating that the line was segregating for this trait) (Table 1). ARGE97-1048-3-6 was homozygous and homogeneous for both molecular markers linked to Fhb3, and lines VA04W-433, ARGE97-1033-10-2 and AR97002-2-1 were heterogeneous for these markers. Lines SZ 14 and AR97002-2-1 were heterogeneous for both markers linked to the 5AS QTL. The remaining resistant lines and the susceptible control (Coker 9835) were homozygous and homogeneous for absence of the markers used in the study.
The phytotoxic effect of DON (bleaching) within spikes was first visible at 7 days after DON application, and symptoms on susceptible lines continued to spread until the experiments ended at 21 days after treatment. Differences among lines were greatest at 21 days (data not shown), and the number of DON-bleached primary florets at 21 days was chosen to represent the phytotoxic effects of DON. Lines were significantly different (P < 0·0001) for the number of DON-bleached primary florets 21 days after treatment, and the six wheat lines with molecular markers linked to Fhb1 had fewer DON-bleached florets than the 10 lines without this gene (Figs 1 & 2). Bleaching did not spread from the four DON-treated florets of lines VA04W-433, NC03-11465, Fg 368 and SZ 13. For line SZ 14, bleaching spread into an average of two additional florets resulting in six DON-bleached primary florets 21 days after treatment (Fig. 1). Lines without Fhb1 averaged from 17 to 30 DON-bleached primary florets. Line ARGE97-1047-4-2, which was heterogeneous for Fhb1, ranked between the groups of lines with and without Fhb1.
There were significant differences (P < 0·0001) among lines for the relative yield of DON-treated spikes. However, lines with Fhb1 did not have higher relative yield than lines without Fhb1 (Fig. 3). Therefore, resistance to DON as measured by the number of DON-bleached florets did not protect plants from the phytotoxic effects of DON on kernel formation as measured by the relative yield of treated spikes. Lines Fg 365 and Fg 368 averaged 50 and 54% relative yield, respectively, and had higher relative yields than other lines that averaged 8–32% relative yield. The average number of primary florets per spike varied among lines from 29 to 48, and there was a weak positive correlation (R = 0·57; P = 0·0206) between relative yield and the number of florets per spike.
The number of DON-bleached florets averaged 18–31 for the lines evaluated in Experiment 2 (Fig. 4). Although there were some significant differences (P = 0·0172) among the lines, the range of values for these lines was similar to the range of values for lines in Experiment 1 that did not have Fhb1. None of the lines in Experiment 2 had Fhb1 or resistance to the phytotoxic effect of DON. There were significant differences (P = 0·0111) among lines for the relative yield of DON-treated spikes (Fig. 5). Petrus had higher relative yield (61%) than Sakura (12%) and Apache (8%), and the remaining lines were intermediate between these extremes and not significantly different from each other. Petrus, Raduza and Darwin had relative yields ≥50%, similar to the relative yields of the highest lines in Experiment 1. The number of primary florets per spike among lines averaged from 34 to 44, and there was no significant correlation (P = 0·1479) between relative yield and the number of florets per spike, indicating that relative yield was not influenced by the size of the spikes.
Results of this study indicate that all six wheat lines with resistance gene Fhb1 have resistance to DON applied to florets at flowering and that 17 lines with other genes for FHB resistance do not have resistance to DON. Lines with Fhb1 usually did not have bleaching symptoms beyond the four primary florets into which DON had been applied, whereas lines without Fhb1 had 17–31 DON-bleached primary florets that equalled 42–78% of the primary florets on spikes. These results support the conclusions of Lemmens et al. (2005) that resistance to DON was associated with Fhb1 and that Fhb1 may code for or regulate the expression of a DON-glucosyl-transferase enzyme that converts DON to DON-3-O-glucoside. Among the FHB resistance genes used in contemporary American and European wheat cultivars and advanced breeding lines, Fhb1 appears to have a unique mode of action because none of the other resistance genes in the lines had a similar phenotype in response to DON application. Given that Fhb1 probably functions by converting DON to the masked mycotoxin, DON-3-O-glucocide, it is important to note that other unknown genes conferring high levels of resistance to spread within a spike have a different mode of action and may not result in the accumulation of DON-3-O-glucocide in harvested grain.
Furthermore, resistance to DON, as determined by the minimal spread of bleaching symptoms from the florets into which DON was applied, did not protect spikes from the phytotoxic effects of DON on kernel formation as measured by the relative yield of treated spikes. Therefore, DON caused damage to kernels beyond what could be measured by visually rating spikes for bleached florets. Fhb1 appears to protect spikes from loss of chlorophyll in the presence of DON but does not protect from toxic effects on kernel formation. Even though wheat lines with Fhb1 performed well in the field or greenhouse, as measured by visual head blight symptoms caused by DON chemotypes of F. graminearum (Pumphrey et al., 2007; Rosyara et al., 2009; Horevaj et al., 2011), yield of these lines may be reduced due to the failure of Fhb1 to protect spikes from the phytotoxic effects of DON on kernel formation in non-infected florets, especially florets above the point of infection. This may explain why soft red winter wheat lines with Fhb1 yield poorly in head blight nurseries (E. A. Milus, University of Arkansas, unpublished data). These findings are supported by the recent work of Bushnell et al. (2010) who determined that DON caused loss of electrolytes from plant cells due to damaged plasma membranes even when there were no bleaching symptoms. These authors concluded that the roles of DON in FHB development are multiple and complex, thereby opening the possibility for host resistance at multiple metabolic processes. In addition, field ratings for head blight severity (percentage of florets blighted) do not always agree with ratings for percentage of fusarium-damaged kernels (Paul et al., 2006), indicating that different mechanisms may control resistance to blighting and resistance to kernel damage.
Lines Fg 365, Fg 368, Petrus, Raduza and Darwin had relative yields ≥50% after treatment with DON, indicating that they may possess one or more genes conferring ability to fill kernels in the presence of DON. All of these lines were of European origin. Mesterházy et al. (1999) reported that line Fg 365 had the highest tolerance against head blight (ability to yield well in the presence of head blight), and measuring the relative yield after DON application may be useful for identifying lines with tolerance. Additional lines with tolerance as determined in field experiments will need to be evaluated for relative yield loss after DON application in order to assess the effectiveness of this method to identify lines for tolerance to head blight.
The low frequency of known FHB resistance genes and QTL among the FHB-resistant wheat lines in this study indicates that there are probably several diverse genes for resistance among these lines. Genes conferring tolerance to DON, as measured by high relative yields following application of DON, may allow higher yields in the presence of head blight and may be most useful in combination with other resistance genes with different modes of action. The results of this study identified likely sources of tolerance to DON and a possible means to identify lines with this trait.
The authors thank David Moon, Peter Rohman and Jody Hedge for technical assistance, Edward Gbur Jr. for statistical advice, and R. Bacon, C. Griffey, A. McKendry, Á, Mesterházy, P. Murphy and O. Veskrna who contributed wheat lines for this study. This material is based upon work supported by the U.S. Department of Agriculture, under Agreement No. 59-0790-9-054. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the U.S. Department of Agriculture.
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