Differential influence of QTL linked to Fusarium headblight, Fusarium-damaged kernel, deoxynivalenol contentsand associated morphological traits in a Frontana-derivedwheat population

Szabo-Hever Agnes • Lehoczki-Krsjak Szabolcs •

Varga Monika • Purnhauser Laszlo •

Pauk Janos • Lantos Csaba • Mesterhazy Akos

Received: 5 November 2013 / Accepted: 17 April 2014

� Springer Science+Business Media Dordrecht 2014

Abstract The genetic background of Fusarium head

blight (FHB) resistance in the moderately resistant

wheat variety Frontana was investigated in the GK

Mini Mano/Frontana DH population (n = 168). The

plant material was evaluated across seven epidemic

environments for FHB, Fusarium-damaged kernel

(FDK) and deoxynivalenol (DON) contents caused

by two Fusarium species (F. culmorum and F.

graminearum). The effects of phenotypic traits such

as plant height and heading date were also considered

in the experiments. In the population, 527 polymorph

markers (DArT, SSR) within a distance of 1,381 cM

distance were mapped. The quantitative trait locus/

loci (QTL) on chromosomes 4A and 4B demonstrated

a significant linkage only with FHB, while QTL on

chromosomes 3A, 4B, 7A and 7B were linked to DON

accumulation alone. Regions determining all the

investigated Fusarium resistance traits were identified

on chromosomes 1B, 2D, 3B, 5A, 5B and 6B. The

markers in these regions are of the greatest signif-

icance from the aspect of resistance breeding. Our

results indicate that the genetic background of

resistance against FHB, FDK and DON accumulation

can differ, and all these traits should be taken under

consideration during resistance tests. Moreover, this is

the first report on the mapping of Frontana-derived

QTL that influence DON accumulation, which is

important since the level of DON contamination

determines the actions of the food and feed industries.

Selection should therefore also focus on this trait by

using molecular markers linked to DON content.

Keywords Triticum aestivum � Fusarium head

blight � Fusarium-damaged kernel �Deoxynivalenol � Quantitative trait loci �Resistance

Introduction

Fusarium head blight (FHB) is one of the most

devastating diseases of wheat (Triticum aestivum L.)

worldwide, mainly in consequence of the harmful

mycotoxins produced by this pathogen. The head

symptoms may be associated with Fusarium-damaged

kernels (FDK), which is important, because the

damaged seeds are the main sources of mycotoxins.

Resistance breeders worldwide have the aim of

finding plant stocks from which FHB resistance could

be transferred into new cultivars. Asian spring wheat

varieties and landraces such as Sumai 3, Nobeoka

Bozu, Wangshuibai and Chokwang are the most widely

investigated resistance sources. Unfortunately, the

Electronic supplementary material The online version ofthis article (doi:10.1007/s10681-014-1124-2) contains supple-mentary material, which is available to authorized users.

S.-H. Agnes (&) � L.-K. Szabolcs � V. Monika �P. Laszlo � P. Janos � L. Csaba � M. Akos

Cereal Research Non-Profit Limited Company, Also

kikot}o sor 9, 6726 Szeged, Hungary

e-mail: agnes.szabo@gabonakutato.hu

123

Euphytica

DOI 10.1007/s10681-014-1124-2

available exotic resistance sources are usually sensitive

to other diseases (e.g. powdery mildew or leaf rust), and

their yield capacities, adaptation abilities and technical

qualities are low. FHB resistance is currently consid-

ered to be race-non-specific (Van Eeuwijk et al. 1995;

Mesterhazy 2002) and species-non-specific (Mester-

hazy et al. 2005; Toth et al. 2008), and is therefore

durable. The improvement of Fusarium resistance in

new varieties primarily demands new sources for more

effective quantitative trait locus/loci (QTL) combina-

tions. This would improve the durability of resistance

(Gervais et al. 2003; Ruckenbauer et al. 2001) and the

possibility of the selection of more aggressive isolates

could be reduced.

The moderately resistant Frontana from Brazil

could well be a good candidate for the discovery of

useful new QTL/molecular markers (Schroeder and

Christensen 1963; Singh et al. 1995; Van Ginkel et al.

1996). This cultivar has both Type I and Type II

resistance, and in vitro experiments have suggested

that Frontana can degrade and tolerate relatively high

levels of deoxynivalenol (DON) content (Miller and

Arnison 1986; Wang and Miller 1988). Steiner et al.

(2004) mapped the FHB resistance (Type I) QTL due

to Frontana on chromosomes 2B, 3A, 4B, 5A and 6B,

and those due to Remus on chromosomes 1B, 2A and

3B in a Frontana/Remus DH population. Szabo-Hever

et al. (2012) carried out a QTL analysis on the same

population with Type I Fusarium resistance data (FHB

and FDK) and found QTL identical with those

published by Steiner et al. (2004) on chromosomes

2B, 3A, 4B, 5A and 6B. These chromosome regions

are therefore most likely to carry stable Frontana-

derived Fusarium resistance QTL. The study by

Szabo-Hever et al. (2012) clearly demonstrated that

the validation of molecular markers is necessary for

breeders to check constantly on the presence of a locus

responsible for an investigated trait. Mardi et al.

(2006) confirmed the existence of the FHB resistance

QTL on chromosome 3AL and identified two addi-

tional QTL on chromosomes 1BL and 7AS in a

Frontana/Falat population. Srinivasachary et al.

(2008) ascribed the FHB resistance QTL on chromo-

somes 1B, 2B, 3A, 6A, 7A and 7D and the plant height

QTL on chromosomes 2B and 5B to the Frontana-

derived RL4137 parent, in a RL4137/Timgalen RIL

population. Berzonsky et al. (2007) identified FHB

resistance QTL due to Frontana on chromosomes 3A,

6A and 4D. The importance of Frontana as a resistance

source was reported by Yang et al. (2006), who

claimed that this variety does not possess a QTL

identical with the Sumai 3 on chromosomes 3B and

6B. This was verified by the experiments of McCart-

ney et al. (2004), who concluded that the fragment

sizes yielded by markers on chromosomes 3BS, 3BSc

and 5A were not identical for Frontana and Sumai 3

(nor most of the other Chinese resistance sources).

This pointed to the fact that Asian resistance sources

have different QTL from those of Frontana. All these

previous mapping results indicate that the resistance in

Frontana is controlled by several QTL with minor

effects. The cited authors concentrated on the visual

head symptoms, while the DON reaction was not

mapped at all and FDK was mapped only by Szabo-

Hever et al. (2012).

FHB resistance may be influenced by different

morphological traits, such as plant height and heading

date (Mesterhazy 1987, 1995; Parry et al. 1995). An

accurate QTL analysis requires a differentiation between

QTL responsible for resistance and those of other

morphological traits influencing the severity of Fusarium

damage. This is important for breeders in order to avoid

the transfer of an undesired morphological trait with

FHB resistance (e.g. pleiotropy or linkage drag), or

instead of it (e.g. false QTL detection) into an elite,

productive variety (Kosova et al. 2009). Phenotyping is

therefore a key issue in QTL analysis, where reduction of

the ‘‘background noise’’ of morphology and other traits

operating disease development is very important.

Mapping of QTL linked to DON content has

become a vital need, since the whole of the food and

feed industries relies on the control of toxin contam-

ination. It is also important for breeders to know

whether the identified Fusarium resistance QTL are

linked to toxin contamination. The primary aim of our

study was (i) to identify Frontana-derived Fusarium

resistance QTL linked to FHB severity, FDK rate and

DON accumulation. (ii) The genetic background of

traits influencing the Fusarium severity (e.g. plant

height and heading date) was also investigated in the

GK Mini Mano/Frontana population. (iii) The results

obtained on this population were compared with those

on the previously investigated Frontana/Remus pop-

ulation in order to validate the detected QTL. (iiii) We

additionally set out to clarify the effects of QTL

influencing one or more resistance traits (FHB, FDK,

or DON), since this might be decisive from the aspect

of utilizing the given QTL in the breeding process.

Euphytica

123

Materials and methods

Plant material

The GK Mini Mano/Frontana DH mapping population

(168 lines) was developed from a cross of ‘GK Mini

Mano’ and ‘Frontana’. Frontana (Fronteira/Mentana)

is a Brazilian spring wheat variety that is moderately

resistant to FHB. In the cross, the sensitive parent was

the GK Mini Mano (Arthur 71/Sava//Rusalka/NS171/

3/F30.74), a former breeding line of the Cereal

Research Non-Profit Ltd. Co. (CRNC; Szeged, Hun-

gary) that is susceptible to FHB. The investigated

population was generated at the Department of

Biotechnology of the CRNC, using anther culture

method (Lantos et al. 2013; Pauk et al. 2003).

Field experiments

The field tests were conducted in 2008 and 2009 in the

nursery of the CRNC (Szeged, Kecskes station;

46�1402400N, 20�503900E). Seeds were sown in autumn

(mid-October), using Wintersteiger Plot Spider seeding-

machine (Wintersteiger GmbH, Ried, Austria). Plots

were sown in a randomized complete block design, with

1.5 m row length, and 12 cm row width. The number of

rows in a plot was set according to the number of isolates

used for inoculation (one row per replicate for an

isolate). Each isolate was used in two replications,

meaning bunches consisting of about 20 heads.

Inoculation procedure

Inoculum production and the inoculation process were

performed by the method of Mesterhazy (1985, 1987,

1995). Isolates were tested for aggressiveness in vitro

prior to inoculation. The names of the isolates used

and their aggressiveness characteristics are listed in

Table 1. In order to inoculate the spikes uniformly,

bunches of 15–25 spikes were sprayed from all sides

with a hand-held sprayer at full flowering (Feekes

growth stage 10.5.1), using about 15–20 ml of fungal

suspension for each sample. In each year, the plant

material was inoculated individually with 3–4 isolates

of either F. graminearum or F. culmorum. Only one

bunch was placed on each row of a genotype. In order

to avoid cross inoculation, a distance of 30–40 cm was

maintained between bunches. After inoculation,

bunches were covered with a transparent polyethylene

bag for 48 h. After removal of the bags, the plants

were loosely bound with a label for identification, the

leaves being allowed to photosynthesize freely.

FHB severity assessment

Observations of the severity of FHB were started on

day 10 after inoculation, and were repeated every

fourth day until the heads turned yellow, which meant

4–5 observations in a vegetation period. The severity

of FHB was estimated in terms of the percentage of

infected spikelets. The FHB severity rates reported

here are means of all observations. From these, the

means for each Fusarium species and for all experi-

ments were also calculated.

FDK rate assessment

Following the manual harvesting of infected bunches,

the samples were threshed with a stationary thresher

(Wintersteiger LD 180, Austria) at low wind, and the

chaff was removed with an Ets Plaut-Aubry air

separator (41290 Conan-Oucques, France), the shriv-

elled, low thousand kernel weight (TKW) Fusarium-

damaged seeds being retained. The percentage of FDK

was next estimated visually.

DON content measurement

DON content was measured in the samples from

experiments 1, 2 and 4 in 2008 and experiments 5 and

6 in 2009. From these experiments, the samples of the

Table 1 Names of isolates and number of conidia/cm3 used in

the field screening in each experiment and the results of the

Petri dish tests (mean percentage of infected germs of five

readings)

Year Experiment Name of

isolate

Number of

conidia/cm3Rate of

infected

seeds (%)

2008 Exp. 1 Fg. 12377 5.7 9 105 13.5

Exp. 2 Fc. 12551 2.2 9 105 30.2

Exp. 3 Fc. 12551 2.2 9 105 30.9

Exp. 4 Fg. 46.06 1.3 9 105 35.8

2009 Exp. 5 Fc. 12551 0.2 9 105 41.0

Exp. 6 Fg. 12377 0a 39.6

Exp. 7 Fg. 13.05 0.2 9 105 47.0

a Only mycelium was present

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123

two replications per genotype were pooled in order to

obtain homogenized samples for the analyses. DON

content was measured by HPLC with a diode array

detector, as described by Mesterhazy et al. (1999).

Assessment of phenotypic traits influencing FHB

In each year, plant height (the distance from the soil

surface to the top of heads excluding the awns) and

lodging (the percentage of lodged plants in a plot)

were measured and date of heading (the number of

days from 1 January to heading) was recorded.

Statistical analysis of the phenotypic traits

Statistical analyses were performed with SPSS 15.0

software (SPSS Inc., Chicago, IL, USA), using the

‘‘Descriptive statistics’’, ‘‘Compare means’’, ‘‘General

Linear Model’’ and ‘‘Correlate’’ functions. The data on

each fungal isolate (F. graminearum or F. culmorum)

from different years were analysed as single experi-

ments (epidemic situations), taking into consideration

the phenomenon that there are no races within the

Fusarium spp. The data were checked for normal

distribution (Weber 1972), and broadsense heritability

was estimated across experiments according to Ny-

quist (1991) with the following formula: H2 across

experiments = 1 - (MSGxE/MSG) (MSGxE: mean

square genotype 9 experiment; MSG: mean square

genotype).

DNA isolation and molecular markers

DNA was isolated from seedling leaf tissue according

to the CTAB method (Rogers and Bendich 1985). The

quality and quantity were measured with a NanoDrop

1000 Spectrophotometer (Thermo Scientific, USA).

To map the GK Mini Mano/Frontana population, a

database of 24 SSR and 619 DArT markers was used.

Most of the SSR primers were selected from the

literature (Mardi et al. 2006; Roder et al. 1998; Somers

et al. 2004; Steiner et al. 2004). In order to validate

Frontana-derived QTL, SSR markers were used which

proved tightly linked to FHB resistance in the

previously investigated Frontana/Remus population

(Szabo-Hever et al. 2012). The DArT marker data

were provided by the Australian Diversity Arrays

Technology Pty Limited (Yarralumla, Australia),

following the ‘‘Wheat PstI(TaqI)’’ genetic analysis.

Molecular mapping and QTL analysis

Linkage groups were constructed by using JoinMap�

3.0 software (Van Ooijen and Voorrips 2001), and

interval mapping was carried out with MapQTL� 5

software (Van Ooijen 2004). The sequence of markers

was set according to the molecular map published on

the GrainGenes (http://wheat.pw.usda.gov/ggpages/

SSRclub/GeneticPhysical/) and by Somers et al.

(2004). To determine the sequence of DArT markers,

the Triticarte database published on the Diversity

Arrays Technology Pty Ltd homepage (http://www.

triticarte.com.au/content/further_development.html)

was used. The molecular maps reported by Detering

et al. (2010) and Semagn et al. (2006) were also used

to determine the marker sequence. Interval mapping

(IM) was performed with the phenotypic data of

single experiments, with the mean of F. graminearum

and F. culmorum inoculations, respectively, and with

the overall means of FHB severity and FDK rates,

and with lodging, plant height and heading date data.

The minimum LOD score was set to 2.0 during the

mapping, but in several experiments the permutation

tests indicated LOD[1.2 as the level of significance

of linkage (Van Ooijen 1999).

Results

In the experiments, 168 DH lines of the GK Mini

Mano/Frontana population were tested in the field for

Fusarium resistance. QTL analysis was performed in a

two-year study, with 3-4 isolates per year. Besides the

traditional visual symptoms, the FDK reaction and,

uniquely, DON contamination were also mapped.

FHB severity, FDK rate and DON content

The overall means of FHB severity, FDK rate and DON

content demonstrated normal distribution across the

investigated experiments (Fig. 1). The parents exhibited

Fusarium severity according to their expected resistance

level. The FHB severity varied between 16.0 and

62.3 %, and the FDK rate between 22.3 and 94.4 %

(overall means). The heritability (H2) value between

epidemic situations was 0.89 for FHB severity and 0.82

for FDK rate, which reveals the good reproducibility of

Euphytica

123

the experiments. The average DON content in the

population (overall means) was between 27.6 and

150.3 mg/kg. The results of descriptive statistical

analysis of the FHB, FDK and DON data are presented

in Table 2. The isolates displayed different levels of

aggressiveness in the field: the most aggressive isolates

A

0

5

10

15

20

25

30

14-1

8

19-2

2

23-2

6

27-3

0

31-3

4

35-3

8

39-4

2

43-4

6

47-5

0

51-5

4

55-5

8

59-6

2

63-6

6

FHB mean (%)

Num

ber

of li

nes Frontana

GK Mini Manó

Mean= 35.3

LSD5%= 0.57

B

0

2

4

6

8

10

12

14

16

18

20

20-2

4

25-2

8

29-3

2

33-3

6

37-4

0

41-4

4

45-4

8

49-5

2

53-5

6

57-6

0

61-6

4

65-6

8

69-7

2

73-7

6

77-8

0

81-8

4

85-8

8

89-9

2

93-9

6

FDK mean (%)

Num

ber

of li

nes

Frontana

GK Mini Manó

Mean= 61.4

LSD5%= 0.93

C

0

5

10

15

20

25

30

35

0-20

21-3

0

31-4

0

41-5

0

51-6

0

61-7

0

71-8

0

81-9

0

91-1

00

101-

110

111-

120

121-

130

131-

140

141-

150

151-

160

161-

170

DON (mg/kg)

Num

ber

of li

nes

Mean = 77.1

LSD5% = 7.29

Frontana

GK Mini Manó

Fig. 1 Distribution of FHB severity (a), FDK rates (b) and DON content (c) in a GK Mini Mano/Frontana DH population as compared

with the values of the parental lines (indicated with arrows). Szeged, 2008–2009

Euphytica

123

were used in experiments 1 (FDK mean: 85.2 %), 2

(DON mean: 194.7 mg/kg) and 4 (FHB mean: 56.2 %),

while the least aggressive isolate was used in experiment

7 (FHB: 22.6 %, FDK: 44.2 %, DON: not investigated).

The variance analysis (ANOVA) confirmed the appro-

priate distribution and variance of the data among the

lines. Large differences in FHB severity, FDK rate and

DON content between the parental genotypes resulted in

significant genetic variations in the mapping population.

The genotype-by-experiment interaction was calculated

for FHB severity and FDK rate across the seven

epidemic situations (Table 3). The genotype effects

differed significantly from the genotype-by-experiment

interaction, indicating that the basic ranking was similar

between the lines throughout the experimental

environments.

Table 2 Means, ranges and standard deviations for FHB severity (%), FDK rate (%) and DON content (mg/kg) caused by isolates of

F. graminearum and F. culmorum over seven environments (experiments) in a GK Mini Mano/Frontana population

Experiment Isolate Trait Frontana GK Mini

Mano

Population

mean

Population

range

SD

Exp. 1 Fg. 12377 FHB 39.3 61.9 52.6 21.4–80.6 12.1

FDK 50.0 93.8 85.2 40–100 11.7

DON 48.2 69.0 68.0 23.6–142.5 20.7

Exp. 2 Fc. 12551 FHB 25.3 50.8 41.3 9.1–75.6 14.0

FDK 43.8 94.3 79.5 20–100 15.7

DON 96.2 244.3 194.7 52.8–492.2 74.8

Exp. 3 Fc. 12551 FHB 6.3 47.1 37.9 4.4–82.5 17.9

FDK 6.0 81.7 61.8 3–98 22.4

DON n.i. n.i. n.i. n.i. n.i.

Exp. 4 Fg. 46.06 FHB 33.2 62.9 56.2 28.9–83.8 12.7

FDK 57.5 90.2 81.5 25–100 13.6

DON 28.2 58.6 58.0 3.6–150.9 22.1

Exp. 5 Fc. 12551 FHB 2.3 30.6 23.0 0.7–54.4 12.2

FDK 0.5 75.0 45.8 0.0–92.5 26.2

DON 0.5 87.2 34.9 0.0–87.5 20.3

Exp. 6 Fg. 12377 FHB 10.1 33.8 25.0 1.7–63.6 13.2

FDK 9.0 67.5 48.6 0.5–96.5 28.4

DON 6.9 50.3 29.6 0.0–76.4 17.7

Exp. 7 Fg. 13.05 FHB 12.5 27.1 22.6 1.5–51.6 11.4

FDK 18.0 74.2 44.2 0.0–98.5 24.5

DON n.i. n.i. n.i. n.i. n.i.

Means F. culmorum FHB 11.3 42.8 33.9 9.3–65.6 12.5

FDK 16.8 83.7 62.0 12.7–95.3 16.9

DON 48.4 165.7 114.8 33.2–258.2 41.0

F. graminearum FHB 23.8 46.4 39.0 19.3–69.4 9.6

FDK 33.6 81.4 64.5 33.6–96.1 14.7

DON 27.8 59.3 52.0 22.5–117.4 14.8

FHB 18.4 44.9 35.3 16.0–62.3 10.3

FDK 26.4 82.4 61.5 22.3–94.4 15.7

DON 36.0 101.9 77.1 27.6–150.3 23.2

Plant height 125 60 90.0 58–133 17.7

Heading date 125 126 127.4 124–138 2.2

Plant height (cm) and heading date (days) are mean values from the experiments investigated

n.i. not investigated

Euphytica

123

Assessment of other phenotypic traits

Wide-ranging differences in plant height were observed

among the lines (ranging from 58 to 133 cm). As both

parents were awned, all lines of the population were also

awned, which made the QTL analysis more exact,

avoiding the influential effect of awnedness on Fusar-

ium severity. The differences in heading date among the

lines were smaller than those observed in the previously

investigated Frontana/Remus population (Szabo-Hever

et al. 2012). This led to the experimental advantage that

the number of inoculations could be reduced to two. The

calculated means, ranges and standard deviations for

these traits are listed in Table 2.

Correlation analysis

Correlations were calculated between the overall means

of FHB severity, FDK rate, DON content, heading date

(HD), plant height (PH) and lodging data (LODG)

(Table 4). Among the traits investigated, the strongest

correlation (0.680) was obtained between the FHB and

FDK data. A strong correlation (0.539) was also found

between the FDK rate and DON content, whereas only

a moderate association (0.319) was detected between

the FHB and DON data (all significant at the 0.001

level). The analysis revealed that the tall genotypes

displayed fewer Fusarium-damage symptoms (FHB: -

0.519 and FDK: -0.512 correlation values at the 0.001

level), and these genotypes also lodged more severely.

This latter phenomenon did not influence the symp-

toms, since the plant material lodged at the end of the

vegetation period. HD influenced FDK and DON to

only a low extent (correlation values 0.247 and 0.425 at

the 0.01 and 0.001 level, respectively), which is

indicative of some fungal growth after the soft dough

stage (Feekes scale: 11.2).

Molecular mapping

From the database of 643 polymorphic DArT and SSR

markers, 527 markers were mapped to 28 groups

covering a genetic distance of 1,381 cM (average

marker distance: 2.62 cM). Chromosome positions of

26 linkage groups were defined amongst the mapped

groups. Linkage groups were mapped on each chro-

mosome except for 3D, 4D and 6D.

QTL detection

QTL analyses were carried out with the data of each

epidemic situation for FHB severity (Supplementary

Table S1), FDK rate (Supplementary Table S2) and

DON content (Supplementary Table S3). The overall

means and mean data of the symptom severity caused

by the two Fusarium species reflected the stable

linkage with the chromosome regions identified

Table 3 Analysis of variance for FHB severity (A), FDK rate

(B) and DON content (C)

Source df MS F-value P

(A) FHB

Experiment (E) 6 65,887.50 2,778.00 \0.0001

Genotype (G) 167 1,519.98 64.09 \0.0001

GxE 999 173.25 7.30 \0.0001

Error 1,173 23.72

(B) FDK

Experiment (E) 6 107,347.06 1,666.22 \0.0001

Genotype (G) 167 3,031.11 47.05 \0.0001

GxE 999 542.93 8.43 \0.0001

Error 1,173 64.43

(C) DON

Experiment (E) 4 768,292.04 675.01 \0.0001

Genotype (G) 167 2,682.65 2.36 \0.0001

Error 668 1138.19

Table 4 Correlations between overall mean of FHB severity, FDK rate, DON content, heading date (HD), plant height (PH) and

lodging data (LODG) (n = 168)

FHB FDK DON HD PH

FDK 0.680***

DON 0.319*** 0.539***

HD 0.092 0.247** 0.425***

PH -0.519*** -0.512*** -0.372*** -0.053

LODG -0.357*** -0.308*** -0.239** -0.134 0.676***

** Correlation significant at the 0.01 level; *** Correlation significant at the 0.001 level

Euphytica

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8.7

6.6

72

3.0

6.6

12

3.0

wP

t-7

32

60

35

.81

14

.36

.60

22

.26

.34

20

.6

wP

t-3

81

2–

wP

t-7

32

41

12

D–

n.s

.n

.s.

n.s

.n

.s.

n.s

.n

.s.

Xg

wm

26

13

.54

8.9

5.0

11

2.4

4.7

31

1.8

Xg

wm

53

3–

wP

t-3

92

13

Bw

Pt-

79

89

70

4.2

51

0.6

3.7

19

.33

.97

10

.0w

Pt-

74

20

60

2.1

35

.52

.83

7.2

2.5

46

.6

wP

t-8

00

50

9–

wP

t-2

78

04

Aw

Pt-

08

04

5.1

01

2.6

6.0

71

4.8

5.7

31

4.6

–n

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n.s

.n

.s.

n.s

.n

.s.

n.s

.

wP

t-5

33

4–

wP

t-4

24

34

Bw

Pt-

62

09

3.2

38

.23

.43

8.7

3.6

09

.1–

n.s

.n

.s.

n.s

.n

.s.

n.s

.n

.s.

Xg

wm

20

5–

Xg

wm

15

65

AX

gw

m2

93

3.5

89

.05

.26

13

.74

.73

12

.2X

gw

m2

93

4.9

71

3.4

3.7

91

0.3

4.7

11

2.7

wP

t-7

41

13

4–

wP

t-5

89

65

Bw

Pt-

72

40

2.4

58

.22

.36

8.1

2.5

48

.7w

Pt-

72

40

4.3

41

4.1

5.4

31

5.0

5.3

41

5.0

wP

t-7

20

4–

wP

t-7

44

78

66

Aw

Pt-

72

04

3.9

91

0.0

3.3

48

.53

.97

10

.5w

Pt-

72

04

5.1

91

2.9

5.5

71

3.7

5.7

91

4.2

wP

t-6

03

9–

Xg

wm

88

6B

Xg

wm

88

7.4

61

8.9

7.4

41

8.7

8.1

42

0.5

Xg

wm

88

5.4

41

3.6

4.4

21

1.3

5.3

11

3.3

wP

t-9

92

5–

wP

t-5

92

27

Bw

Pt-

56

46

3.1

37

.93

.55

9.6

3.5

21

0.8

wP

t-4

04

56

.28

15

.34

.32

10

.85

.67

13

.9

wP

t-0

93

4–

wP

t-7

43

60

17

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n.s

.n

.s.

n.s

.n

.s.

n.s

.n

.s.

wP

t-7

43

60

12

.79

7.1

2.8

47

.33

.12

7.9

Xg

wm

44

–w

Pt-

74

42

19

NA

1X

gw

m4

42

.51

6.5

3.5

49

.03

.33

8.5

Xg

wm

44

2.7

17

.01

.45

3.8

2.1

65

.6

wP

t-6

66

59

3–

wP

t-6

64

68

2N

A2

wP

t-6

64

68

22

.08

5.6

2.0

15

.42

.21

7.6

wP

t-6

64

68

22

.84

10

.12

.96

10

.43

.18

11

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Euphytica

123

(Tables 5, 6). The LOD values in the QTL regions

varied between the experiments, but all the QTL

introduced in this study demonstrated a significant

linkage with an investigated trait. Analyses were also

performed with the experimentally observed HD

(Table 7) and PH (Table 8) data. The linkage groups

and the QTL regions identified are shown in Fig. 2 and

by means of LOD curves in Supplementary Fig. S1.

QTL linked to FHB were identified on chromo-

somes 1A, 1B, 2D (wPt-732882–wPt-667765), 3B,

4A, 4B, 5A, 5B, 6A, 6B and 7B and in two unassigned

chromosome regions. The highest LOD value (8.14)

was observed on chromosome 6B, explaining 20.5 %

of the phenotypic variance (r2 or VE).

QTL on chromosomes 1A, 1B, 2D (wPt-732882 -

wPt-667765, wPt-3812 - wPt-732411), 3B, 5A, 5B,

6A, 6B, 7B and 7D and in two unassigned chromo-

some regions were linked to resistance against FDK.

The strongest association was found on chromosome

2D (wPt-732882–wPt-667765) with a LOD value of

6.34, explaining 20.6 % of the phenotypic variance (r2

or VE).

The QTL were associated with the DON content on

chromosomes 1B, 2D (wPt-732882–wPt-667765,

wPt-3812–wPt-732411), 3A, 3B, 4B, 5A, 5B, 6B,

7A, 7B and 7D. The highest LOD value (4.53) was that

on chromosome 5B, explaining 15.2 % of the pheno-

typic variance (r2 or VE).

All QTL which influenced Fusarium resistance in

our experiments originated from the Frontana variety.

Among the other phenotypic traits, QTL linked to

HD was identified on chromosomes 2B (from GK

Mini Mano), 6A and 7B (from Frontana). The QTL on

chromosomes 1A (wPt-666607), 2B and 3A proved to

be associated with PH alone, while the QTL on 1A

(wPt-734078–wPt-731843), 1B, 2D, 3B, 4A, 4B, 5A,

5B, 6A, 6B, 7B and 7D were associated with both PH

and FHB and/or FDK. The groups of lines bearing the

allele of the GK Mini Mano in these chromosome

regions were significantly shorter than the lines in the

groups bearing Frontana alleles.

Table 6 Locations of the detected QTL and chromosome regions with LOD values and percentages of explained phenotypic

variance (VE) for DON content

Marker; map interval Chromosome Peak DON

F. c. F. g. Mean

LOD VE LOD VE LOD VE

wPt-9857–wPt-2315 1B wPt-0705 2.42 6.2 2.11 5.7 2.78 7.1

wPt-732882–wPt-667765 2D wPt-733932 4.37 10.9 2.10 5.4 4.12 10.3

wPt-3812–wPt-732411 2D Xgwm261 1.97 5.1 2.41 6.5 2.49 6.4

wPt-0286–wPt-5886 3A wPt-1562 1.87 7.1 2.89 9.3 2.67 9.3

Xgwm533–wPt-3921 3B wPt-2757 4.43 11.1 2.13 5.5 4.01 10.1

wPt-732448–wPt-6869 4B wPt-3439 2.56 7.5 1.57 4.1 2.58 7.5

Xgwm129 5A Xgwm129 2.11 5.9 1.39 3.6 2.14 5.5

wPt-2586–wPt-5896 5B wPt-7240 3.77 12.6 3.56 12.1 4.53 15.2

Xgwm88 6B Xgwm88 2.88 7.4 0.97 3.1 2.48 6.6

wPt-7763–wPt-1601 7A wPt-1601 2.29 5.9 1.45 3.8 2.28 5.9

wPt-9467–wPt-5283 7B wPt-7318 3.06 8.8 3.40 10.0 3.85 10.3

wPt-0934– wPt-743601 7D wPt-743601 2.69 6.9 3.13 8.0 3.41 8.7

F.c.: mapping results, considering the data of Fusarium culmorum isolates; F.g.: mapping results, considering the data of Fusarium

graminearum isolates

Table 7 Locations of the detected QTL and chromosome

regions with LOD values and percentages of explained phe-

notypic variance (VE) for heading date

Marker; map

interval

Chromosome Peak Heading

date

LOD VE

wPt-4664–wPt-7715 2B wPt-3561 4.28 11.1

wPt-741026–wPt-

744786

6A wPt-

744786

2.17 5.7

wPt-5283–wPt-7318 7B wPt-7318 3.37 12.3

Euphytica

123

Discussion

The identified QTL regions are discussed in the

sequence of numbered wheat chromosomes, aided by

the chromosome illustrations (Fig. 2 and Supplemen-

tary Fig. 1).

Two QTL regions were identified on chromosome

1A. The marker region wPt-734078—wPt-731843

was linked to FHB, FDK and PH, while wPt-666607

was linked to only PH. Fusarium resistance QTL are

rarely mentioned on this chromosome, and a QTL with

a similar effect in the Frontana variety has never been

published previously.

Paillard et al. (2004) and Schmolke et al. (2008)

described a QTL on chromosome 1B linked to PH and

FHB, while Srinivasachary et al. (2008) identified only

FHB QTL on chromosome 1BS, which was not linked

to PH in a Frontana-derived RL4137. However, the

similarities of these QTL with those identified in our

experiment as influencing FHB, FDK, DON and PH

are questionable. Our data suggest that there must be

two QTL in close proximity on chromosome 1B,

affecting Fusarium resistance and PH. The Frontana-

derived FHB QTL identified by Mardi et al. (2006) on

chromosome 1B did not overlap with that described in

our experiment.

The HD QTL in the wPt-4664–wPt-7715 and the

PH QTL in the wPt-4664–wPt-3132 marker region on

chromosome 2B were not associated with any Fusar-

ium resistance trait. In the Frontana/Remus popula-

tion, a PH QTL was identified by Steiner et al. (2004)

and Szabo-Hever et al. (2012) in this region. However,

(2008) and Steiner et al. (2004) found that this QTL

was linked to both PH and FHB. These results lead us

to presume that there must be three QTL in close

proximity in this chromosome segment, linked to

Fusarium resistance, PH and HD. The effects of this

QTL region might be explained by the Eps (earliness

per se) (Scarth and Law 1983) or by the Ppd-B1

(photoperiod response) (Law et al. 1978; McIntosh

et al. 2010; Scarth and Law 1983) genes. The PH QTL

on the long arm of chromosome 2B (wPt-8916–wPt-

5736) has not been detected earlier.

Handa et al. (2008) and Heidari et al. (2012)

detected the Rht8 dwarfing gene and a MRP (multi-

drug resistance protein) gene in the proximity of the

QTL linked to FDK, DON and PH on chromosome 2D

(wPt-3812–wPt-732411). This FHB resistance QTL

has not been identified in Frontana previously. The

QTL on the same chromosome in the wPt-732882–

wPt-667765 marker region was found to influence

FHB, FDK, DON and PH in our experiments. In the

phenotypically more homogeneous Frontana/Remus

population, only a Fusarium resistance QTL (derived

from Frontana) has been detected in this chromosome

segment (Szabo-Hever et al. 2012).

Table 8 Locations of the detected QTL and chromosome

regions with LOD values and percentages of explained phe-

notypic variance (VE) for plant height

Marker; map

interval

Chromosome Peak Plant height

LOD VE

wPt-666607 1A wPt-

666607

3.05 7.9

wPt-734078–wPt-

731843

1A wPt-

734027

2.67 7.0

wPt-0325–wPt-

2315

1B wPt-2575 6.07 14.9

wPt-4664–wPt-

3132

2B wPt-2228 5.91 14.5

wPt-8916–wPt-

5736

2B wPt-8916 3.57 9.0

wPt-732882–wPt-

667765

2D wPt-

732603

2.14 7.7

wPt-3812–wPt-

732411

2D Xgwm261 3.97 10.3

wPt-9268–wPt-

1694

3A wPt-4398 3.44 8.8

Xgwm533–wPt-

3921

3B wPt-3921 4.31 19.3

wPt-0804 4A wPt-0804 2.08 5.3

wPt-8892–wPt-

5303

4B wPt-6209 3.03 7.7

Xgwm205–

Xgwm156

5A Xgwm293 5.31 13.3

wPt-1409–wPt-

5896

5B wPt-4628 3.39 9.3

wPt-7204–wPt-

744786

6A wPt-7204 3.65 10.8

wPt-6039–

Xgwm88

6B Xgwm88 4.03 12.9

wPt-9925–wPt-

1266

7B wPt-8040 2.99 7.7

wPt-0934–wPt-

743601

7D wPt-0934 4.52 11.3

cFig. 2 QTL linked to FHB (empty bar), FDK (black bar), DON

content (crossed bar), plant height (PH; right-striped bar) and

heading date (HD; left-striped bar) in the GK Mini Mano/

Frontana population. ND not defined

Euphytica

123

Euphytica

123

Fig. 2 continued

Euphytica

123

Fig. 2 continued

Euphytica

123

A Fusarium resistance QTL on chromosome 3A

has been repeatedly validated in Frontana (Mardi

et al. 2006; Steiner et al. 2004; Szabo-Hever et al.

2012). However, in our experiments this QTL in

the wPt-0286–wPt-5886 marker region was linked

only to the DON content, while another one

between the markers wPt-9268–wPt-1694 was

associated with PH. All these findings are in line

with the results of Borner et al. (2002) and Mao

et al. (2010), who presumed two QTL on chromo-

some 3A which influence FHB and PH in other

wheat populations.

Fig. 2 continued

Euphytica

123

The QTL linked to FHB, FDK, DON and PH on

chromosome 3B (Xgwm533–wPt-3921) overlapped

with the position of the often investigated Fhb1 locus.

As previous findings affirmed the lack of this locus in

the Frontana variety (Buerstmayr et al. 2009; Szabo-

Hever et al. 2012), the effect of morphological

resistance is strongly presumed in this case. Another

explanation might be the existence of more than one

FHB resistance QTL close to each other in this region,

with different levels of effectiveness.

An FHB QTL and a PH QTL were detected on

chromosome 4A (wPt-800509–wPt-2780, wPt-7280).

Our assumption that there are two different loci

influencing these traits is strengthened by the results of

Borner et al. (2002), who identified only a PH QTL in

this region, and by the fact that only an FHB QTL was

previously detected in this position of the Frontana

variety (Steiner et al. 2004; Szabo-Hever et al. 2012).

The QTL influencing the DON content on chromo-

some 4B (wPt-732448–wPt-6869) is unique, since it

was not linked to any other Fusarium resistance trait in

our experiments, and it has not been detected as an

FHB resistance QTL in any other Frontana-derived

population earlier. The FHB (wPt-5334–wPt-4243)

and the PH (wPt-8892–wPt-5303) QTL—mapped in

the other region of 4B—were also present in the

Frontana/Remus population in the experiments of

Steiner et al. (2004), while Szabo-Hever et al. (2012)

found that this locus was responsible for FHB and

FDK resistance, but not for PH in the same population.

It should be mentioned that in this latter experiment a

‘‘bagging’’ inoculation method was used, which

eliminates the effect of differences in PH more

precisely. Overlapping FHB and PH QTL have been

described on chromosome 4B several times, in other

wheat varieties too, but it has still not been clarified

whether linkage or pleiotropy is in the background of

this phenomenon (Draeger et al. 2007; Ma et al. 2008;

Srinivasachary et al. 2009).

The QTL on chromosome 5A (Xgwm205–

Xgwm156) is the best characterized Frontana-derived

Fusarium resistance QTL. In our experiments this

FHB, FDK and DON QTL overlapped with the marker

region influencing PH. This result is in line with that

reported in the Frontana/Remus population by Steiner

et al. (2004). With the bagging inoculation method,

however, Szabo-Hever et al. (2012) found only

Fusarium resistance QTL on chromosome 5A. The

effects of two different QTL in this chromosome

region—one responsible for Fusarium resistance and

the other influencing PH—are supported by findings

from other wheat populations (Draeger et al. 2007;

Jiang et al. 2007; Ma et al. 2008; Mao et al. 2010;

Somers et al. 2003).

On chromosome 5B, QTL linked to FHB, FDK,

DON and PH were also identified. This chromosome

region was mapped to FHB resistance, HD and PH

QTL by Klahr et al. (2007) in the Cansas variety, while

Srinivasachary et al. (2008) found that this region was

linked only to PH and not to FHB in a Frontana-

derived wheat line. These results point to the situation

that there might be three QTL in this region: one

responsible for FHB resistance, one influencing HD

(probably the effect of the Vrn-B1 gene) and one

linked to PH.

Fusarium resistance QTL on chromosome 6A (near

the centromere) has previously been mapped in Dream

and Frontana varieties and in a Frontana-derived line

(Berzonsky et al. 2007; Schmolke et al. 2005;

Srinivasachary et al. 2008). However, these QTL are

most likely not in a similar position to those we

identified influencing FHB, FDK HD and PH in

Frontana in our experiments. However, Mao et al.

(2010) and Paillard et al. (2004) mapped FHB

resistance and PH QTL on the long arm of chromo-

some 6A.

We mapped FHB, FDK, DON and PH QTL on

chromosome 6B in the region where the Fhb2 locus

was positioned by Cuthbert et al. (2007). The occur-

rence of two different QTL influencing Fusarium

resistance and PH is strengthened by the results of

Mao et al. (2010). The PH QTL originates from the

susceptible GK Mini Mano, which explains why the

Fusarium resistance QTL did not overlap a locus,

influencing PH in the Frontana/Remus population in

the experiments of either Steiner et al. (2004) or

Szabo-Hever et al. (2012).

A unique QTL linked only to DON content was

identified on chromosome 7AL (wPt-7763–wPt-

1601). This QTL is at a short distance from that

identified by Steiner et al. (2004) in the Frontana/

Remus population, associating spike compactness.

Several Fusarium resistance QTL have been identified

on the long arm of this chromosome in different

resistance sources (Buerstmayr et al. 2009). However,

Srinivasachary et al. (2008) identified a DON QTL in a

Frontana-derived line on chromosome 7AS in a

position similar to that detected by Mardi et al.

Euphytica

123

(2006) linked to FHB in the Frontana variety. This last

QTL region on the short arm of 7A has so far been

detected only in Frontana.

One locus associated with DON content and HD,

and another one linked to FHB, FDK and PH were

detected on chromosome 7B. Lin et al. (2008),

Schmolke et al. (2005) and Szabo-Hever et al.

(2012) also identified two different loci influencing

Fusarium resistance and HD in different plant mate-

rials, among them the Frontana variety. The effect of

the PH QTL may be explained by the Rht9 or Rht13

dwarfing genes, mapped earlier to chromosome 7BS

(Ellis et al. 2005; McIntosh et al. 2010). Similarly, the

HD QTL is in the region where the Vrn-B3 (vernal-

ization response gene) and Eps genes have been

positioned (Flood and Halloran 1983; Yan et al. 2006).

This is the first report of FDK, DON and PH QTL

on chromosome 7D, since this marker region (wPt-

0934–wPt-743601) has previously not been described

to be responsible for any of these traits.

Conclusions

A comparison of our data with those on other

Frontana-derived population reveals several consis-

tent QTL (Berzonsky et al. 2007; Mardi et al. 2006;

Steiner et al. 2004; Szabo-Hever et al. 2012). The

mapping result of Frontana/Remus and GK Mini

Mano/Frontana DH populations reveals that the

Fusarium resistance QTL on chromosomes 2D, 4A,

4B, 5A, 6B and 7B are the most stable, all deriving

from the Frontana variety (Steiner et al. 2004; Szabo-

Hever et al. 2012). Unlike the Frontana/Remus

population, where 3-5 inoculations were applied,

depending on the season (Szabo-Hever et al. 2012),

in the GK Mini Mano/Frontana population this

number could be decreased to two. Moreover, the

weather conditions were similar in the two experi-

mental years (2008 and 2009). This significantly

reduced the ‘‘background noise’’ and made the QTL

analysis more precise, resulting in higher LOD values

and stable QTL detection.

Our results support the importance of using more

Fusarium isolates in different environments since the

strength of linkage in the identified QTL regions

among the single experiments was variable. Further, a

mean result, calculated from more data will furnish an

accurate resistance level, and hence can contribute to a

more precise phenotyping and QTL analysis.

It was surprising that so many QTL proved to

influence plant height in the experiment. This result

will initiate more research with a view to clarifying the

role of plant height and its genetic influence, including

examinations of the presence and effects of Rht genes.

In Fusarium resistance breeding, marker-assisted

selection requires molecular markers which do not

link to any negative agronomic or quality traits.

Additionally, the effects of morphological traits such

as plant height and heading date should also be taken

into account during Fusarium resistance QTL map-

ping. In our experiments, several Fusarium resistance

QTL overlapped with those responsible for morpho-

logical traits. It is difficult to distinguish these loci,

even though the existence of both types of QTL was

verified by earlier published results in most cases.

These observations lead us to draw attention to

morphological traits—especially plant height—during

the breeding process. Our results on the molecular

mapping of Fusarium resistance QTL in the GK Mini

Mano/Frontana population suggest that the use of

marker-assisted selection together with a morpholog-

ical selection is strongly advised.

Several QTL influenced only one of the traits

tested, while some significantly influenced each of

FHB, FDK and DON, and it is therefore recommended

that all of these resistance traits should be analysed.

The information published in this paper will hopefully

prove useful for breeders to combat DON contamina-

tion more effectively. QTL that influence only one

trait might seem to be less important, though they do

influence disease development somehow. From resis-

tance breeding aspects, the markers linked to QTL

influencing a number of traits appear to be the most

useful.

It is very difficult to reach a high Fusarium

resistance level in plants as it is a quantitative trait

influenced by numerous minor QTL, some of which

are still unidentified in the genome. Our results

indicate that phenotyping is a key feature of QTL

analyses. The wheat-Fusarium interaction is very

sensitive and much work is needed to attain the

acceptable reproducibility of the results.

Acknowledgments This research was realized in the frames of

TAMOP 4.2.4. A/1-11-1-2012-0001, National Excellence

Program—Elaborating and operating an inland student and

Euphytica

123

researcher personal support system . The project was subsidized

by the European Union and co-financed by the European Social

Fund. The research was also funded by the MycoRed FP7

project.

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