Journal of Economic Entomology, XX(XX), 2020, 1–8

doi: 10.1093/jee/toz357
Plant Resistance Research

Mapping Quantitative Trait Loci for Resistance to Fall

Armyworm (Lepidoptera: Noctuidae) Leaf-Feeding

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Damage in Maize Inbred Mp705
E. D. Womack,1,3 W. P. Williams,1 J. S. Smith,1 M. L. Warburton,1 and D. Bhattramakki2
USDA-ARS CHPRRU, P.O. Box 9555, Mississippi State, MS 39762, 2Corteva Agriscience™, P.O. Box 1000, Johnston, IA 50131, and
1

Corresponding author, e-mail: [email protected]

3

Subject Editor: Louis Hesler

Received 5 September 2019; Editorial decision 9 December 2019

Abstract
The fall armyworm, Spodoptera frugiperda (J. E. Smith), is an agronomically important pest that severely limits
maize (Zea mays (Linnaeus) [Poales: Poaceae]) production. This migrant insect devastates maize plants in many
countries threatening the livelihood of millions. Quantitative trait loci (QTL) were mapped to identify chromo-
somal regions that control resistance to fall armyworm leaf-feeding and to identify molecular markers linked
to the target loci for use in marker-assisted selection (MAS). A bi-parental mapping population, comprising
243 F2:3 families from the cross Mp705 (resistant) × Mp719 (susceptible), was evaluated for fall armyworm leaf-
feeding damage under artificial infestation over 3 yr. A linkage map comprised of 1,276 single-nucleotide poly-
morphism and simple sequence repeat molecular markers was constructed. Quantitative trait loci analyses
identified two major QTL in bins 4.06 and 9.03 that when combined, explained 35.7% of the phenotypic vari-
ance over all environments. Mp705 was responsible for the leaf-feeding damage reducing alleles for both large
effect QTL and most of the small effect QTL identified in this study. The QTL identified in bin 9.03 co-locates
with a previously identified QTL that controls resistance to leaf-feeding damage in maize by fall armyworm and
other lepidopteran insects. The QTL in bin 4.06 is a new source of resistance identified in this study. Beneficial
alleles derived from Mp705 for the application of an integrated QTL-MAS approach could accelerate breeding
efforts to minimize fall armyworm leaf-feeding in maize.

Key words: insect-feeding damage, host-plant resistance, high-density genetic mapping, single-nucleotide polymorphism

Fall armyworm, Spodoptera frugiperda (J. E. Smith), an inherent armyworm was confirmed in nearly 40 countries in Africa and had
insect pest of tropical-subtropical regions of the Americas, feeds also spread to India and Yemen (FAO 2018). By 2019, this migrant
in large numbers on a broad range of host plants (Sparks 1979). pest ravaged maize plants in all countries of sub-Saharan Africa (46
Although the fall armyworm has a widespread consumption of of Africa’s 54 countries) and 17 Asian countries including Bangladesh,
over 80 plant species including key crops, sorghum (Sorghum bi- China, Myanmar, Sri Lanka, and Thailand (CABI 2019, FAO 2019).
color L. (Moench) [Poales: Poaceae]), cotton (Gossypium hirsutum There are expectations for this pest to spread even farther, causing
L. [Malvales: Malvaceae]), and rice (Oryza sativa L. [Cyperales: significant injury to many other important crops (Early et al. 2018).
Poaceae]), its preferred host plant, however, is maize (Zea mays Considerable efforts were taken in the Americas to develop insect
(Linnaeus) [Poales: Poaceae]) (USAID 2018). A valued crop, maize resistant maize lines during the 1970s to 1990s through conventional
ranks first among all cereal crops produced in the United States breeding (Mihm et al. 1988). The USDA Agricultural Research Service
and it is a paramount crop in many other countries (Martinez and (USDA-ARS, Mississippi) developed and released a series of maize
Fernandez 2019). The fall armyworm is a major threat to this pro- inbred lines with resistance to fall armyworm including Mp496,
duction largely due to its propensity for long-distance dispersal and Mp701-708, Mp713, Mp714, and Mp716 (Williams and Davis 1980,
its aggressive, polyphagous nature. 1982, 1984, 2000, 2002; Scott and Davis 1981; Scott et al. 1982;
In January 2016, outbreaks of the fall armyworm were reported Williams et al. 1990), derived primarily from germplasm held by the
in central and western Africa. A reported 20–50% maize yield loss International Maize and Wheat Improvement Center (CIMMYT,
caused a state of emergency to be declared in some countries (Goergen Mexico). CIMMYT developed populations as well as tropical and
et al. 2016, Early et al. 2018, Banson et al. 2019). By 2018, the fall subtropical maize inbred lines, CML59-74 and CML121-127, from

Published by Oxford University Press on behalf of Entomological Society of America 2020. 1

This work is written by (a) US Government employee(s) and is in the public domain in the US.
2 Journal of Economic Entomology, 2020, Vol. XX, No. XX

USDA-ARS germplasm, with fall armyworm and southwestern corn Materials and Methods
borer, Diatraea grandiosella Dyar (Lepidoptera: Crambidae) resist-
Population Development and Phenotyping
ance (CIMMYT 1998). Breeding programs deploying native host-
plant resistance (HPR) as a safe, cost-effective control method play The mapping population was derived from a cross between the re-
a critical role among all pest management strategies against insect sistant inbred, Mp705 (Williams and Davis 1984), and insect suscep-
predation on agricultural crops (Sharma and Ortiz 2002). However, tible inbred, Mp719 (Williams and Windham 2012) and evaluated
conventional breeding for fall armyworm resistance was no longer a for fall armyworm leaf-feeding damage after artificial infestation. To
top priority after the introduction of Bacillus thuringiensis (Bt) maize generate this population, the F1 was self-pollinated to create F2 seed
in the United States in mid-1990s (Prasanna 2017). Bt maize had and the F2 plants were self-pollinated to produce 243 F2:3 families.
Field trials were conducted in each environment characterized by

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revolutionized pest control, but the large-scale acceptance of Bt trans-
genic maize hybrids over the decades has imposed high selection pres- years 2016, 2017, and 2018 at the R. R. Foil Plant Science Research
sure, resulting in the development of insect resistance to maize, thus Center, Mississippi State, Mississippi. The 2016 test, planted on
reducing pest control efficacy (Da Silva et al. 2016). April 29, included 205 families phenotyped in two replications and
Because transgenic maize is still not commonly adopted in the 2017 (planted April 21) and 2018 (planted May 3) tests included
Africa (ISAAA 2018) and Bt maize may be unable to control the 243 families phenotyped in three replications. The resistant (Mp705)
fall armyworm in the future, accelerated efforts to intensively and susceptible (Mp719) parents and their F1 hybrid (Mp705 ×
screen maize germplasm lines, identify new sources of resistance, Mp719) were included as controls of the experiment in each test.
and utilize native HPR in maize breeding programs are immedi- Experiments were shown in 5.1-m-long single-row plots with 0.96 m
ately needed to improve and develop maize cultivars with native between rows. Plots were arranged in a randomized complete block
fall armyworm resistance to leaf-feeding damage. Initial attempts design with 20 plants per plot.
to transfer insect resistance from donor cultivars to agronomically Fall armyworm neonate larvae were obtained from the insect
acceptable germplasms were met with challenges due to the poor rearing laboratory at the USDA-ARS, Corn Host Plant Resistance
agronomic qualities of the donors and the polygenic nature of the Research Unit (CHPRRU) at Mississippi State. The fall armyworm
trait (Widstrom et al. 1992). The advent of marker-assisted selection neonate larvae were reared according to the procedures of Davis
(MAS) has made it possible to reduce many issues caused by linkage (1989). Within 24 h after fall armyworm eggs hatched, the first-
drag of unfavorable agronomic characteristics (Cobb et al. 2019) instar larvae were mixed with sterile corn-cob grits. The mixture was
and enhance efficiency of selection of target traits. Identification of distributed into the whorl of the maize plants using a hand-operated
molecular markers linked to quantitative trait loci (QTL) encoding dispenser (Davis and Williams 1980). Each maize plant was artifi-
maize resistance to insect pests can facilitate MAS to complement cially infested with ~30 fall armyworm neonates during the mid-
and enhance conventional breeding efforts (Hoisington et al. 1996). whorl stage of growth (approximately V7). Individual plants in a
A few studies have investigated genomic regions encoding maize plot were rated to determine the degree of feeding injury to leaves
resistance to fall armyworm leaf-feeding damage using family-based using a visual scale from 0 (no visible damage) to 9 (severe damage)
QTL analyses. Using 91 simple sequence repeat (SSR) markers on 14 d after infestation as adapted from Davis et al. (1992). The mean
213 F2:3 families, the cross of A619 (susceptible parent) × Mp708 per plot was calculated across 20 plants. The control plants were
(resistant parent) was mapped and analysis revealed QTL found on also evaluated accordingly.
chromosomes 1, 2, 6, 7, and 9 that contributed to resistance (Brooks
et al. 2007). An initial genetic linkage map was created with 231 Statistical Analysis of Phenotypic Data
F2:3 families from the cross of Mp704 (resistant) × Mo17 (suscep- Statistical analyses on the fall armyworm leaf-feeding ratings for the
tible) by Brooks et al. (2005) using 73 SSR markers; this was ex- control genotypes (Mp705, Mp719, and the F1 hybrid) of the ex-
panded by Womack et al. (2018) to a total of 224 single-nucleotide periment were performed in SAS 9.4 (SAS Institute 2014). Each year
polymorphism (SNP) and SSR markers. Quantitative trait loci on at the Mississippi location was treated as an environment (2016,
chromosome bins 1.09, 2.08, 3.08, 6.02, 7.04, 8.03, 9.03, 10.02, and 2017, and 2018). Analysis of variance (ANOVA) was applied to the
10.04 were identified and QTL effects were estimated. Southwestern control genotypes using PROC MIXED across all environments.
corn borer and sugarcane borer (Diatraea saccharalis F.), two other Genotype, environment, genotype-by-environment interaction, and
major lepidopteran pests of maize for which QTL mapping has been block nested in environment were the random effects of the model.
completed, also implicated common genomic regions conferring in- Best linear unbiased predictors (BLUPs) for each family (geno-
sect leaf-feeding resistance in maize (Bohn et al. 1996, 1997, 2001; type) mean were computed using the PROC MIXED procedure in
Groh et al. 1998; Khairallah et al. 1998). However, a restricted SAS 9.4 (SAS Institute 2014). Genotype and block were computed as
number of molecular markers, ranging from 98 to 146 restriction random effects of the model within an environment. Across all en-
fragment length polymorphism (RFLP) markers were used to develop vironments, genotype, environment, genotype-by-environment inter-
these linkage maps, which could lead to inaccurate estimates of QTL action, and block nested in environment were the random effects
and limited application in MAS (Utz et al. 2000, Chen et al. 2017). of the model. Estimates of variance components for the F2:3 family
Currently, high-density linkage maps constructed with SNP-based (genotype) means were obtained along with estimates for the en-
marker technology is easier to obtain (Deschamps et al. 2012). The vironment, genotype-by-environment, block nested in environment,
utilization of more molecular markers allows more precise mapping, and error terms. These BLUP estimates were used for QTL analyses.
estimation of genetic effects, and identification of QTL closely linked to Broad-sense heritability (h2) estimates were calculated from the vari-
molecular markers, all of which are pertinent to improve the efficiency ance components according to Holland et al. (2003).
of MAS. The current study used 1,276 SSR and SNP markers to iden-
tify QTL with resistance to leaf-feeding damage by fall armyworm in
243 F2:3 families from a cross between Mp705 (resistant) and Mp719 Genomic DNA Isolation
(susceptible). Additionally, Mp705, not directly related to Mp704 and Leaf tissue was collected from 20 plants per F2:3 family from field
Mp708 that were previously mapped for fall armyworm leaf-feeding grown (families 1–205) or greenhouse grown (families 206–243)
resistance, may offer a different source of resistance. plants in 2016. One leaf was collected by hand from each plant and
Journal of Economic Entomology, 2020, Vol. XX, No. XX 3

bulked to form a composite sample. Leaf tissue samples were frozen the fragmented DNA. The pellet was resuspended in hybridization
in liquid nitrogen and stored in a freezer at −80°C until they could be buffer and dispensed onto BeadChips. These were hybridized over-
lyophilized using the FreeZone 6 Liter Benchtop Freeze Dry System night at 48°C. The DNA annealed to locus-specific 50-mers during
(Labconco, Kansas City, MO) for 72 h. They were then ground to a hybridization and unhybridized DNA was washed off. The nucleo-
fine powder using a grinding mill (Foss Tecator, Eden Prairie, MN). tides on the BeadChip were stained in Te-Flow (Tecan flow-through)
A modified cetyltrimethylammonium bromide (CTAB) method de- chambers and then single-base extension occurred. The BeadChip
scribed by Saghai-Maroof et al. (1984) was used to extract DNA from was scanned with the iScan reader used to excite the fluorophores.
each composite sample. The quantity and purity of DNA were assessed The genotypic data were extracted from intensity data files using the
using a NanoDrop Spectrophotometer ND-1000 (Thermo Fisher Illumina GenomeStudio Genotyping Module.

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Scientific, Wilmington, DE). DNA samples were diluted to 200 ng/µl
with TE buffer and stored in the −80°C freezer pending genotyping. Linkage Map Construction
The JoinMap 4.0 (Van Ooijen 2006) software was used to develop
Genotyping the genetic linkage map with an F2 population type. The dataset
Simple sequence repeat primers, obtained from Integrated DNA consisted of 1,481 SNP and SSR markers for 243 F2:3 families. The
Technologies (IDT, Coralville, IA) and chosen from MaizeGDB frequencies of the genotypes, according to the expected Mendelian
(MaizeGDB.org), were amplified by polymerase chain reaction genotypic ratio of 1:2:1 (A:H:B), were analyzed using χ 2 statistics for
(PCR) in a 96-well plate performed in 15-µl reactions containing: each marker to assess the observed genotypic ration to identify seg-
7.5-µl RedTaq ReadyMix (Sigma–Aldrich Co., Saint Louis, MO), regation distortion. Markers were excluded if there was missing data
5-µl template DNA (10 ng/µl), 1.5-µl ddH2O, and 0.5-µl (10 nmol) (>10%), high χ 2 values that led to disruption of the marker order,
of each forward and reverse primers. The PCR thermal cycler was markers 100% identical to other loci, and if a marker had a strong
programmed for initial denaturation at 94°C for 2 min; 34 cycles of: linkage outside of its own group. The logarithm of the odds (LOD)
denaturation (94°C for 1 min), annealing (55–58°C for 1 min), and score of the independence test statistic was used to assign markers
elongation (72°C for 2 min); and a final extension at 72°C for 2 min. for linkage grouping. The maximum likelihood-based mapping algo-
The PCR products were loaded on 4% agarose-TBE gel containing rithm (Jansen et al. 2001) was used to calculate recombination fre-
ethidium bromide and run at 105 V for 2–3 h depending on the quencies, marker order, and compute their distances based on the
size of the amplicon. Polymorphic, co-dominant SSR markers were Haldane (1919) mapping function measured in centimorgan (cM).
scored visually from imaged gels obtained using the AlphaImager HP The physical positions of the SSR markers were confirmed through
system (Protein Simple, San Jose, CA). MaizeGDB, maize B73 RefGen v.3 assembly (www.maizegdb.org).
KASP SNP assays (LGC Genomics) are based on two ‘kompetitive’ The physical positions of the SNP markers were confirmed according
allele-specific forward primers each labeled with a different universal to expected allele positions provided by LGC Genomics and Illumina.
FRET (fluorescent resonance energy transfer) tag and one common
reverse primer (Smith and Maughan 2015). KASP assays were per- QTL Mapping
formed in-house in a 384-well plate format, and consisted of 25 ng Quantitative trait loci were detected by Windows QTL Cartographer
dehydrated DNA, 2.5-µl dH2O, 0.07-µl KASP assay primers, and v. 2.5 software (Wang et al. 2012). Composite interval mapping
2.5-µl KASP 2× reaction mix (LGC Genomics, Teddington, UK). (CIM) was performed using cofactor selection of five markers iden-
A ‘touchdown’ PCR program was performed for amplification. tified by forward and backward step-wise regression. These cofac-
After an initial denaturation step at 94°C for 15 min, 10 cycles of tors controlled genetic background noise in other regions of the
touchdown PCR: denaturation (94°C, 20 s) and annealing (65°C genome outside of the 10 cM window that could affect QTL detec-
until a touchdown to 57°C decreasing 0.8°C per cycle over 60 s) tion (Jansen and Stam 1994, Zeng 1994). The genome was scanned
followed by 26 cycles of standard two-step PCR at the lower an- for putative QTL at a walk speed of every 1 cM. Likelihood ratio
nealing temperature of 55°C were performed on an ABI ProFlex (LR) thresholds for genome-wide significance (α = 0.05) were calcu-
thermal cycler (Applied Biosystems, ThermoFisher Scientific) and lated by 1,000 permutation shuffles (Doerge and Churchill 1996).
cooled to 10°C before analysis. The fluorescence signals were de- Significant QTL were declared when the QTL peaks exceeded the
tected on a FLUOstar Omega microplate reader (BMG-Labtech, permutation-based threshold.
Ortenberg, Germany) and data were obtained using MARS Data Terms from the model identified with CIM were used to initiate
Analysis software (BMG-Labtech). The results were viewed graphic- multiple interval mapping (MIM) modeling (Kao and Zeng 1997,
ally as genotyping clustering plots using the KlusterCaller software Kao et al. 1999). Multiple interval mapping allowed for the best
(LGC Genomics). fitted model to explain the observed phenotypic variation without
Genotyping, per Illumina’s protocol (Infinium LCG Assay overfitting the model. Multiple interval mapping was also used to
Protocol Guide 2015), was also performed on a tailored Infinium estimate QTL position while allowing for analysis of epistasis, gen-
array using a 768-plex maize assay (Jones et al. 2009) coupled to etic effects, and genotypic values to predict phenotypic values for
Illumina’s MaizeLD BeadChip array (Rousselle et al. 2015) (services individual families (Kao et al. 1999). The criterion selection was
courtesy of Corteva Agriscience, Johnston, IA). DNA sample set to an LOD threshold of 3.6 with a minimum LOD from peak
(200 ng) was denatured with sodium hydroxide and neutralized to to baseline of 1.6 and a minimum distance between QTL of 5 cM
prepare for amplification. For genome amplification, the master mix along the chromosome. A model was selected according to Silva
was added to the plate and samples were incubated overnight at et al. (2012) based on the Bayesian information criterion (BIC).
37°C in the Illumina Hybridization Oven (Illumina, San Diego, CA) These steps were repeated until additional terms could not be added
generating enough DNA to be used for the assay. An enzyme-based to a model, without overfitting by exceeding the heritability esti-
method was used to fragment the amplified product and endpoint mated from the variance components. The genetic effects (additive,
fragmentation was used to avoid over-fragmentation. DNA was pre- dominance, and epistasis) from the final model, genotypic predicted
cipitated with isopropanol and precipitation solution. The samples value, and the estimates of the variance explained by QTL were de-
were centrifuged at 3,000 × g at 4°C for 20 min to obtain a pellet of termined. The signs of the genetic effect were used to identify the
4 Journal of Economic Entomology, 2020, Vol. XX, No. XX

parent contributing the allele influencing leaf-feeding damage by the the maize genome. The markers were assigned to linkage groups
fall armyworm (Lübberstedt et al. 1997) and the magnitudes of the and LOD scores of 3.0 were used to create the groups; 10 groups
genetic effect were also estimated. remained associated even at the most stringent level of the test,
LOD = 10.0. The number of markers per linkage group ranged from
40 to 233 markers. The total length of the Mp705 × Mp719 map
Results was 1,642 cM, with an average interval of 1.3 cM between markers
Phenotypic Performance of Parental Lines and F2:3 and the largest interval of 16.8 cM. Chromosome 3 showed some
Families significant deviation from the expected 1:2:1 Mendelian ratio for an
F2 segregating population where the alleles from Mp719 were trans-
When evaluated for leaf-feeding damage by the fall armyworm, the

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mitted more frequently than the alleles from Mp705.
overall means (±SE) across 2016, 2017, and 2018 for Mp705 (re-
sistant parent), Mp719 (susceptible parent), and the F1 hybrid were
3.95 ± 0.43, 6.77 ± 0.31, and 4.42 ± 0.56, respectively. Results of QTL Analysis
the ANOVA across all environments, showed that block nested in Initial MIM models were built based on the models obtained from
environment was not significant (F = 1.74; df = 5; P = 0.2127). The CIM analysis (Supp Table 2 [online only]). Using MIM, a step-
effect due to genotype by environment was significant (F = 9.84; wise search for QTL identified genetic models containing six QTL
df = 4; P = 0.0017) and the main effects were not interpreted but a in 2016, 10 QTL and three interactions in 2017, and four QTL
test of simple effects by environment was performed using multiple in 2018. Data over all environments revealed six QTL and one
comparisons of the mean fall armyworm leaf-feeding ratings of the interaction were identified (Table 2). These models explained 54.0
control genotypes (Table 1). In every environment, Mp705 (resistant (2016), 61.8 (2017), 46.5 (2018), and 56.6% (average across the
parent) had a significantly lower rating than the Mp719 (susceptible three environments) of the total phenotypic variances. There were
parent). The F1 hybrid was developed by breeding the genotypes of individual QTL that were responsible for >10% of the total pheno-
its inbred parents. In 2016, the data appeared to fit a dominance typic variance in 2016, 2018, and across all environments. A QTL in
model toward the susceptible parent. In 2017, the F1 hybrid showed bin 9.03 (58.2–60.91 cM) that explained a significant portion of the
superior performance over both parents. In 2018, the data appeared phenotypic variance was observed in 2016 (26.6%), 2018 (26.0%),
to fit an additive model where the leaf-feeding damage rating of F1 and across all environments (22.5%). An individual QTL in bin 1.11
hybrid fell between the resistant and susceptible parents but, the F1 explained 11.2% of the phenotypic variance in 2016. A novel QTL
was not statistically different from the resistant parent and the sus- in bin 4.05–4.06 explained 8.6, 8.7, 7.5, and 13.2% of the total
ceptible parent (Table 1). The additive and dominant effects may not phenotypic variance in 2016, 2017, 2018, and across all environ-
be the same for each environment due to genotype-by-environment ments, respectively.
interactions. Genetic parameters were estimated by MIM that allowed the
The overall means for the families when analyzing fall armyworm identification of beneficial (fall armyworm leaf-feeding damage re-
leaf-feeding damage in each environment were 4.22 ± 0.05 (2016), ducing) alleles. Both inbred lines, Mp705 (resistant) and Mp719
4.37 ± 0.04 (2017), and 5.64 ± 0.05 (2018). The BLUP estimates (susceptible), contributed alleles that decreased fall armyworm leaf-
were calculated for each 243 F2:3 family in every environment feeding damage, but the majority of favorable alleles were supplied
and over all the environments. Covariance parameters were esti- by Mp705. Mp719 was responsible for the fall armyworm leaf-
mated using BLUP analysis in PROC MIXED. In each environ- feeding damage reducing alleles for QTL in bins 1.02 and 4.03 in
ment, 2016 (z = 5.03; P < 0.0001), 2017 (z = 6.94; P < 0.0001), and 2016, bin 1.02 in 2017, and bin 1.03 across all environments. In all
2018 (z = 5.20; P < 0.0001), there were significant genetic differ- cases where Mp719 gave the beneficial allele, those QTL explained a
ences among family means. Across all environments (4.75 ± 0.46), smaller portion of the phenotypic variance in their respective models
ANOVA showed that the effect due to block nested in environment (Table 2). The largest effects were in bin 9.03 (additive, −0.329)
was not significant (z = 1.56; p < 0.0599) but the variance due to the in 2016, bin 6.01 (additive, −0.207) in 2017, bin 9.03 (additive,
genotype-by-environment interaction was highly significant (z = 3.9; −0.310) in 2018, and bin 9.03 (additive, −0.275) across all envir-
p < 0.001). The broad-sense heritability estimates calculated from onments and the origin of the fall armyworm leaf-feeding damage
the variance components within each environment and over the reducing allele was Mp705, the resistant parent, in every case.
three environments ranged from 0.50 to 0.63. Once the final model is selected and all parameters estimated,
the genotypic values of individual families can be estimated for use
Linkage Map Construction in MAS. The genotypic value of each family was estimated based on
The linkage map had a distribution of 1,276 SSR and SNP markers the trait phenotype and marker genotypes, Q and q from the Mp705
(Supp Table 1 [online only]) representing all 10 chromosomes in and Mp719 alleles, respectively (0 = qq, 1 = Qq, 2 = QQ; Zeng

Table 1. Multiple comparisons of the mean leaf-feeding ratings of the control genotypes by environments

MS 2016 MS 2017 MS 2018

Genotype Leaf-feedinga Genotype Leaf-feeding Genotype Leaf-feeding

Mp719 5.60a Mp719 6.99a Mp719 7.32a

F1 5.58a Mp705 4.72b F1 5.45ab
Mp705 2.60b F1 2.66c Mp705 4.07b

MS, Mississippi.
a
Mean leaf-feeding rating, based on a scale from 0 (no damage) to 9 (severe damage), followed by the same letter are not significantly different at α = 0.05.
Journal of Economic Entomology, 2020, Vol. XX, No. XX 5

Table 2. Multiple interval mapping results within and across all environments for fall armyworm leaf-feeding damage

Effect Phenotypic variance

Environment Chromosome bin QTL Peak position 2-LOD interval Aa Db A D Total

cM %
MS 2016 1.02 63.3 62–69.1 0.134 0.013 2.7 −0.1 2.6
1.11 206.5 202.8–211.1 −0.220 −0.005 11.2 0.0 11.2
4.03 39.7 34.1–46.3 0.182 0.064 −0.8 0.5 −0.3
4.05 57.2 57.2–57.2 −0.248 0.031 8.6 0.0 8.6

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4.09 124.5 112.5–133.2 −0.139 −0.131 4.5 0.8 5.3
9.03 58.2 56–61.7 −0.329 0.096 25.6 1.0 26.6
54.0
MS 2017 1.02 51.4 46.5–54.6 0.087 −0.078 0.0 0.7 0.7
1.07 136.8 131.3–154.7 −0.120 0.003 4.2 0.0 4.2
1.09 175.8 167.2–194.2 −0.099 −0.128 3.3 1.6 4.9
2.04 75.2 69.2–76.6 −0.165 −0.057 4.6 0.6 5.2
4.06 73.6 69.5–77.4 −0.170 −0.056 8.2 0.5 8.7
6.01 18.8 16.2–30.6 −0.207 0.069 7.7 0.7 8.4
8.02 27.2 21.9–31.8 −0.153 −0.109 5.1 1.3 6.4
9.04 74.5 72.8–80.2 −0.115 −0.211 3.1 4.1 7.2
10.02 26.1 18–34.5 −0.155 0.060 4.9 −0.1 4.8
10.07 95.1 86.4–100.1 0.069 −0.184 0.7 3.0 3.7
1.02 × 4.06 −0.269 (DA) 3.0 3.0
2.04 × 9.04 0.306 (DD) 1.5 1.5
2.04 × 8.02 0.191 (AA) 3.1 3.1
61.8
MS 2018 1.10 189.61 181.8–191.6 −0.196 0.048 8.3 0.2 8.5
3.01 49.71 33.9–58.4 −0.024 −0.171 0.5 4.0 4.5
4.06 79.11 70–80.2 −0.157 −0.092 5.8 1.7 7.5
9.03 60.91 52–62.9 −0.310 0.122 23.8 2.2 26.0
46.5
All 1.03 65.31 60.2–74.2 0.119 −0.065 2.2 0.8 3.0
1.09 178.31 175.8–175.8 −0.182 −0.080 9.1 0.3 9.4
4.06 75.61 69.3–83 −0.179 −0.119 11.1 2.1 13.2
7.03 73.51 72.3–76.4 −0.101 −0.062 1.7 0.2 1.9
9.03 60.91 56–62.8 −0.275 0.021 22.4 0.1 22.5
10.02 26.11 19.8–30.7 −0.161 0.018 5.0 0.0 5.0
1.09 × 10.02 −0.099 (AA) 1.6 1.6
56.6

MS, Mississippi; QTL, quantitative trait loci; LOD, logarithm of odds; A, additive; D, dominance
a
A negative additive effect indicates Mp705 is the source of the beneficial (fall armyworm leaf-feeding damage-reducing) allele, and a positive additive QTL
effect indicates the resistance is contributed by Mp719.
b
A negative effect indicates that dominance is in the direction of the fall armyworm leaf-feeding damage-reducing allele, no matter which parent is the source,
and a positive effect indicate that dominance is in the direction of the fall armyworm leaf-feeding damage-increasing allele.

et al. 1999). The 10 best families for data across all environments, as can only be accomplished by increasing the number of progeny, and
ranked by genotypic value and by phenotypic value, are provided in thus potential recombinants, in the mapping population. The cur-
Table 3. Table 3 also contains some families whose phenotypic per- rent map, based on fewer than 250 progenies of Mp705 × Mp719,
formance differ greatly from their estimated genotypic values. has enough markers to reliably detect QTL, but possibly insufficient
numbers of progeny for accurate fine mapping.
The validation and fine mapping of a common QTL region in dif-
Discussion ferent genetic backgrounds is also essential for use in MAS to enhance
Breeding efforts for genetic improvement using MAS in maize has breeding efficiency (Langridge et al. 2001). The QTL in bin 9.03 (58.2–
been hampered by an insufficient number of molecular markers in 75.4 cM) was found in this study in a similar location as QTL for
some QTL mapping projects, resulting in low genetic resolution and insect leaf-feeding found in previous studies with other genetic back-
imprecise estimates of QTL effects (Cerrudo et al. 2018). In the cur- grounds (Bohn et al. 1996, 1997; Groh et al. 1998; Khairallah et al.
rent study, a high-density genetic linkage map of Mp705 × Mp719 1998; Willcox et al. 2002; Brooks et al. 2005, 2007; Womack et al.
was constructed to identify the position of QTL for resistance to 2018). Following validation, this large-effect QTL may be targeted for
fall armyworm leaf-feeding damage as suggested by Su et al. (2017). MAS introgression breeding and is expected to perform consistently
With 1,276 markers covering 1,642 cM, the present map is almost in new genetic backgrounds. The large effect QTL from Mp705 in
the same length as the IBM (B73 × Mo17) framework map of 1,725 bin 4.05–4.06 (57.2–79.7 cM), identified in every environment of this
cM (Ganal et al. 2011). Once sufficient markers have been added study, was not identified in previous studies and offers a new genetic
to a map to prevent large gaps, further accuracy and fine mapping source of resistance for fall armyworm leaf-feeding in maize.
6 Journal of Economic Entomology, 2020, Vol. XX, No. XX

Table 3. Families ranked by estimated genotypic value and by phenotypic value when data are across all environments

Family Phenotypea Phenotypic rank QTL genotypeb Genotypic valuec QTL effectd Genotypic rank

Ranked by genotypic value

101 3.93 5 121122 3.94 −0.82 1
142 3.95 7 112122 4.08 −0.68 2
149 4.17 22 221222 4.08 −0.67 3
212 4.53 67 022112 4.13 −0.63 4
64 4.56 72 122212 4.14 −0.62 5
82 4.31 39 122112 4.18 −0.58 6

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241 3.83 2 121221 4.18 −0.58 6
159 3.99 9 121121 4.22 −0.54 8
17 4.74 121 121121 4.22 −0.54 8
100 3.80 1 112022 4.24 −0.52 10
Ranked by phenotypic value
100 3.80 1 112022 4.24 −0.52 10
241 3.83 2 121221 4.18 −0.58 7
181 3.91 3 111111 4.62 −0.14 83
110 3.92 4 102121 4.52 −0.24 54
101 3.93 5 121122 3.94 −0.82 1
151 3.93 5 111121 4.32 −0.44 17
142 3.95 7 112122 4.08 −0.68 2
204 3.95 7 121021 4.38 −0.38 28
159 3.99 9 121121 4.22 −0.54 8
152 4.02 10 122211 4.42 −0.34 31
163 4.02 10 011011 4.72 −0.04 117

QTL, quantitative trait loci.

a
BLUP of insect ratings estimated from data across three environments.
b
Multi-locus QTL genotypes estimated from marker genotypes and trait phenotypes (Zeng et al. 1999). Q and q denote the Mp705 and Mp719 allele, respect-
ively: 0 = qq; 1 = Qq; 2 = QQ.
c
The weighted sum of the genotypic values for all possible QTL genotypes, weighted by the probability of each QTL genotype conditioned on the marker and
phenotypic data (Zeng et al. 1999). Genotypic values are estimated according to Cockerham’s model (Cockerham 1954, Kao and Zeng 2002).
d
QTL effects expressed as a deviation from the population mean.

Other studies have identified QTL for maize resistance to insects; The dense genetic linkage map created in this study allowed for
these provide a framework for the ability to pyramid multiple QTL the identification of several major chromosomal regions harboring
for resistance to the same insects (i.e., fall armyworm resistance important QTL to control leaf-feeding damage by fall armyworm
from Mp708 (Brooks et al. 2007)); or similar leaf-feeding insects in maize. The two largest QTL (one in the same genomic location
(i.e., European corn borer (Ostrinia nubilalis Hübner [Lepidoptera: as that found in other mapping populations and a novel QTL iden-
Crambidae]) resistance from Mo47 (Jampatong et al. 2002); Asian tified here) together explain ~37% of the phenotypic variance for
corn borer (Ostrinia furnacalis Guenée [Lepidoptera: Crambidae]) this trait. Using the flanking markers presented in this study, maize
resistance from Mc37 (Xia et al. 2010); southwestern corn borer breeders can use MAS to introgress these two QTL into susceptible
resistance from Mp708 (Brooks et al. 2007) and CML139 maize hybrid parents in order to control this destructive pest.
(Khairallah et al. 1998); and sugarcane borer (Diatraea saccharalis
Fabricius [Lepidoptera: Crambidae]) resistance from CML67 (Bohn
et al. 1996, 1997; Groh et al. 1998). In these studies, there were Supplementary Data
overlapping regions of QTL located on chromosome 9 (bin 9.01– Supplementary data are available at Journal of Economic
9.05) with QTL found on chromosome bin 9.03 identified in the Entomology online.
current study. This common region could provide greater opportun-
ities for breeders to improve resistance against leaf-feeding insect in
maize using MAS. Acknowledgments
Despite the existence of several published QTL mapping studies We thank Jack Haynes, Susan Wolf, and Gerald Matthews for their
that identified resistant genotypes, a very limited number of studies skilled technical assistance and Corteva Agriscience for providing
have shown the effective application of QTL-based MAS in practical genotyping services. We would like to express our gratitude to the
breeding programs in maize (Ragot and Lee 2009). Successful intro- internal reviewers for their effort and expertise that they contributed
gression of the QTL region on chromosome 9.03 with a phenotypic to reviewing our manuscript. We also would like to thank the USDA-
variance of 17.3% originating from CML67 (resistant donor parent) ARS for supporting this research. This research was funded by the
into CML204 (susceptible recurrent parent) was achieved Willcox United States Department of Agriculture, Agriculture Research
et al. (2002), who found a significant improvement in resistance fol- Service, Project Number: 6064-21000-015-00D. Mention of trade
lowing introgression of the QTL into susceptible genotypes. Of the names or commercial products in this publication is solely for the
10 families with the highest genotypic values listed in Table 3, 5 are purpose of providing specific information and does not imply rec-
also within the top 10 highest phenotypic values and would be ideal ommendation or endorsement by the United States Department of
breeding material for fall armyworm resistance. Agriculture.
Journal of Economic Entomology, 2020, Vol. XX, No. XX 7

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