Livestock Science 233 (2020) 103943

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Livestock Science
journal homepage: www.elsevier.com/locate/livsci

Genome association of carcass and palatability traits from Bos indicus-Bos T

taurus crossbred steers within electrical stimulation status and
correspondence with steer temperament 3. Aroma and flavor attributes of
cooked steaks
D.G. Riley , C. Mantilla-Rojas, R.K. Miller, K.L. Nicholson, C.A. Gill, A.D. Herring, P.K. Riggs,
⁎

J.E. Sawyer, J.W. Savell, J.O. Sanders

Department of Animal Science, Texas A&M University, College Station 77843, USA

ARTICLE INFO ABSTRACT

Keywords: Steaks from Bos indicus-influenced steers (n = 350) were evaluated for beef flavor and aromatic traits. Electrical
Angus stimulation status was a fixed effect. Genome-wide association was conducted with 34,957 SNP from a com-
Crossbreeding mercial array using a mixed linear model. Significant effects of electrical stimulation were less intense acid and
Electrical stimulation browned flavors, and more intense cooked beef lean and livery flavors (P < 0.05). There were no strong simple
Flavor
or residual correlations among the flavor traits with carcass quantity, quality, sensory panel palatability, or
Nellore
temperament traits of steers. There were 18 (no electrical stimulation; chemical burn, cooked beef lean, livery,
sour) and 8 (electrical stimulation; acid, chemical burn, cooked beef lean, metallic) SNP associated with flavor
traits (FDR < 0.18). Closest genes to these were involved in neural/neuronal processes or cellular and extra-
cellular structure.

1. Introduction characterization of inheritance of flavor traits, and to identify SNP and

The value and quality of beef may be supported by aspects of flavor
and aroma that are difficult to quantify (Kerth and Miller, 2015).
Substantial effort to identify important flavors and aromatics of beef
has permitted investigation of an additional level of palatability
(Adhikari et al., 2011). Relationships among these types of traits as well
as with carcass quantity, quality, and other beef palatability traits are
mostly not known. Electrical stimulation may alter flavor in unexpected
ways. Limited genetic assessment of these kinds of traits has been
conducted; genomic regions or loci were identified that were statisti-
cally associated with beef flavor and odor or abnormal beef flavor or
odor (Gutiérrez-Gil et al., 2008). Gill et al. (2009) reported a single SNP
within the gene growth hormone receptor on BTA 20 associated with beef
odor. Otherwise, assessments have been for more traditional sensory
panel measures such as beef flavor intensity or other characterization of
degree of acceptable or unacceptable flavor (e.g., Dang et al., 2014).
This is the third in a series of three reports. The objectives were to
evaluate the effect of electrical stimulation status on flavor traits, assess
simple and residual correlations of flavor traits with other beef traits
and with steer temperament, assess family structure as a broad
candidate genes that associate with these traits.
2. Materials and methods
2.1. Animals
Animal use protocols were approved by the Texas A&M University
Institutional Animal Care and Use Committee. Steers (n = 350) used in this
project were produced in designed F2 Nellore-Angus embryo transfer full-
sibling and natural mating half-sibling families sired by the same 4 F1
Nellore-Angus bulls. Further details regarding management, feeding, and
slaughter procedures for these steers were described in the first of these
manuscripts (Riley et al., 2019). The right side of each carcass was subjected
to electrical stimulation as a series of 550 V (AC) impulses (17; each 1.8 s
with pauses of 1.8 s) and 2 to 6 A for 1 min within an hour of slaughter.
2.2. Traits evaluated
Cooked steaks from each carcass side were prepared consistent with
AMSA (2016) guidelines and evaluated by trained panels for the

⁎
Corresponding author.
E-mail address: david-riley@tamu.edu (D.G. Riley).

https://doi.org/10.1016/j.livsci.2020.103943
Received 11 November 2019; Received in revised form 23 January 2020; Accepted 24 January 2020
Available online 29 January 2020
1871-1413/ © 2020 Elsevier B.V. All rights reserved.
D.G. Riley, et al. Livestock Science 233 (2020) 103943

Table 1
Aroma and flavor attributes and definitions.
Trait Description

Acid Fundamental taste on tongue associated with acids

Bitter Fundamental taste factor associated with a caffeine solution
Bloody/Serum Aromatics associated with blood on cooked meat products
Browned Aromatic associated with the outside of grilled or broiled meat; seared but not blackened or burnt
Burnt Sharp, acrid flavor note associated with over roasted beef muscle, something over baked or excessively browned in oil
Cardboard Aromatics associated with slightly oxidized fats and oils, reminiscent of wet cardboard packaging
Chemical Aromatics associated with garden hose, hot Teflon pan, plastic packaging and petroleum based products such as charcoal lighter fluid.
Chemical burn Chemical feeling factor associated with high concentrations of irritants to the mucous membranes of the oral cavity
Cooked beef lean Amount of beef flavor identity
Cooked beef fat Aromatics associated with cooked animal fat
Cowy Aromatics associated with old beef flavor
Dirt Aromatics characteristic of dry mud, dirt, or soil
Fishy Aromatics associated with trimethylamine and old fish
Grassy Sharp slightly pungent aromatics associated with green/plant/vegetable matter such as parsley, spinach, pea pod, fresh cut grass, etc.
Livery Aromatics associated with cooked organ meat/liver
Metal Flat chemical feeling factor stimulated on the tongue by metal coins
Metallic Impression of slightly oxidized metal, such as iron, copper, and silver spoons
Milky Aromatics associated with products made from cow's milk, such as cream, milk, sour cream or butter milk
Musty Musty, sweet, decaying vegetation; dark damp-musty-earthy note
Nutty Nutty characteristics include sweet, oily, light brown, slightly musty and/or buttery, earthy, woody, astringent, bitter, etc.
Old Aromatics associated with closed air spaces such as attics, closets (dry), and basements (wet)
Salt Fundamental taste factor of which sodium chloride is typical
Serum/broth Flat, salty, somewhat brothy
Smoke Dry, dusty aromatic reminiscent of burning wood
Soda Taste factor associated with sodium bicarbonate as that in baking soda, or a saltless saltine cracker
Soapy Aromatics commonly found in unscented hand soap
Sour Fundamental taste factor associated with a citric acid solution
Soured Sour, fermented aromatics associated with dairy products such as buttermilk and sour cream
Sweet Fundamental taste factor associated with a sucrose solution

Table 2 Table 3
Summary statistics for sensory traits of steaks from carcass sides subjected to Summary statistics for sensory traits of steaks from carcass sides not subjected
electrical stimulation. to electrical stimulation.
Trait n Mean SD Min Max Non-0 scores Trait n Mean SD Min Max Non-0 scores

Acid 311 2.11 0.356 1 2.83 311 Acid 339 2.046 0.37 0.5 3 339
Bitter 311 2.087 0.216 1.4 2.67 311 Bitter 339 2.113 0.244 1.4 2.8 339
Bloody/Serum 311 2.118 0.419 0.75 3 311 Bloody/Serum 339 2.099 0.446 1 3.25 339
Browned 311 0.526 0.463 0 2.4 232 Browned 339 0.584 0.572 0 2.8 247
Burnt 311 0.002 0.028 0 0.5 1 Burnt 339 0.002 0.027 0 0.5 1
Cardboard 311 0.019 0.109 0 1 12 Cardboard 339 0.011 0.066 0 0.6 9
Chemical 311 0.045 0.132 0 0.8 38 Chemical 339 0.076 0.181 0 1 60
Chemical burn 311 0.032 0.099 0 0.5 33 Chemical burn 339 0.05 0.126 0 0.6 52
Cooked beef fat 311 1.693 0.273 1 2.5 311 Cooked beef fat 339 1.682 0.299 1 2.5 339
Cooked beef lean 311 5.064 0.431 4.17 6.4 311 Cooked beef lean 339 4.983 0.493 3.5 7 339
Cowy 197 0.004 0.04 0 0.5 2 Cowy 225 0.002 0.033 0 0.5 1
Dirt 197 0 0 0 0 0 Dirt 225 0.004 0.047 0 0.5 2
Fishy 197 0.007 0.044 0 0.33 5 Fishy 225 0.002 0.016 0 0.167 2
Grassy 311 0.094 0.178 0 0.8 83 Grassy 339 0.099 0.179 0 0.8 95
Livery 311 0.107 0.204 0 1.25 90 Livery 339 0.065 0.142 0 1.25 73
Metal 311 0.084 0.192 0 1 56 Metal 339 0.095 0.209 0 1.25 65
Metallic 311 2.542 0.281 1.75 3.25 311 Metallic 339 2.535 0.292 1.75 3.33 339
Milky 311 0.009 0.054 0 0.4 8 Milky 339 0.011 0.06 0 0.5 12
Musty 311 0.019 0.1 0 0.75 12 Musty 339 0.018 0.095 0 0.8 13
Nutty 311 0.01 0.062 0 0.5 8 Nutty 339 0.006 0.047 0 0.5 5
Old 311 0.007 0.061 0 0.8 5 Old 339 0.001 0.018 0 0.33 1
Salt 311 1.221 0.311 0.5 2.2 311 Salt 339 1.209 0.302 0.5 2.2 339
Serum/broth 311 0.002 0.025 0 0.4 2 Serum/broth 339 0.003 0.031 0 0.4 2
Smoke 197 0.002 0.029 0 0.4 1 Smoke 225 0 0 0 0 0
Soapy 311 0.001 0.013 0 0.167 2 Soapy 339 0.002 0.019 0 0.25 3
Soda 311 0.006 0.039 0 0.4 7 Soda 339 0.006 0.035 0 0.25 10
Sour 311 2.036 0.419 1 3 311 Sour 339 2.028 0.479 0.5 3.333 339
Soured 311 0.012 0.087 0 1.2 9 Soured 339 0.014 0.078 0 0.6 11
Sweet 311 0.015 0.073 0 0.5 15 Sweet 339 0.019 0.078 0 0.5 22

presence and degree of aromatics or off-flavors (Adhikari et al., 2011;
Kerth and Miller, 2015). Values for each were obtained from 9 trained
panelists and averaged. Trait descriptions are provided in Table 1, and
summary statistics for these traits are shown in Tables 2 and 3, from
steaks from electrically stimulated and non-electrically stimulated
sides, respectively.
2.3. Statistical analyses
2.3.1. Model effects
These main effects and their interactions were investigated in pre-
liminary models: year of birth (2003 through 2007), season of birth
(fall, spring), breed type (F2 Nellore-Angus [all produced by embryo

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D.G. Riley, et al. Livestock Science 233 (2020) 103943

Table 4 Table 7
Means for flavor traits by electrical stimulation status. Correlation coefficients (r) of unadjusted (first row for each trait) and residual
values (second row) for flavor traits paired with carcass traits.
Trait Electrical stimulation None P
Longissimus
Acid 2.08 ± 0.028 2.03 ± 0.027 0.023
Bitter 2.08 ± 0.019 2.11 ± 0.018 0.084 Trait Skeletal Carcass area area/ Fat thickness % KPH Yield
Browned 0.47 ± 0.028 0.57 ± 0.026 0.004 maturity weight 100 grade
Cooked beef lean 5.05 ± 0.04 4.97 ± 0.039 0.011 kg
Livery 0.1 ± 0.01 0.06 ± 0.009 0.004
Acid –0.04 –0.17 –0.07 0.16 –0.04 –0.14 –0.15
0.01 –0.02 0.00 0.03 –0.02 –0.04 –0.05
Bitter 0.09 –0.13 –0.04 0.13 0.09 –0.14 –0.13
Table 5
0.02 –0.05 0.00 0.06 –0.09 –0.05 –0.12
Family means for flavor traits.
Bloody/ 0.05 –0.04 0.01 0.07 0.05 0.00 0.02
Sire Family Acid Bitter Cooked Cooked Metal serum 0.00 –0.04 –0.03 0.03 0.03 0.04 0.00
beef fat beef lean Browned 0.06 0.15 0.08 –0.12 0.06 0.06 –0.01
–0.02 –0.05 0.02 0.06 –0.09 0.04 –0.06
297J 70 2.00 2.05 1.74 5.03 2.54 Chemical –0.18 –0.30 –0.19 0.20 –0.18 –0.05 –0.13
71 2.05 2.09 1.68 4.97 2.56 –0.11 0.00 –0.01 –0.01 –0.08 0.06 –0.04
95 2.06 2.09 1.75 5.12 2.50 Chemical –0.15 –0.36 –0.23 0.22 –0.15 –0.09 –0.15
432H 72 1.87b 2.06 1.66 4.98 2.48 burn –0.07 –0.05 –0.06 –0.01 –0.07 0.07 –0.03
73 2.04 2.05 1.56 4.93 2.68 Cooked 0.00 0.16 0.08 –0.13 0.00 0.02 0.06
82 2.10 2.26 1.66 5.05 2.62 beef 0.05 0.12 0.06 –0.08 0.03 0.03 0.03
96 2.07 2.08 1.76 5.10 2.53 fat
437J 74 2.21 2.15 1.65 4.99 2.45 Cooked –0.04 0.12 0.05 –0.10 –0.04 0.09 0.06
75 1.99 2.01 1.72 5.02 2.36b beef 0.02 0.11 0.09 –0.04 0.10 0.12 0.08
81 2.10 2.15 1.64 4.99 2.57 lean
83 2.06 2.05 1.74 5.00 2.50 Grassy 0.02 –0.12 –0.10 0.06 0.02 –0.04 –0.10
97 2.12a 2.08 1.61 4.96 2.56 0.04 –0.03 0.01 0.05 –0.05 –0.04 –0.07
551G 76 2.16 2.17 1.81 4.72 2.57 Livery –0.03 0.05 0.10 0.02 –0.03 –0.05 –0.03
77 2.00 2.13 1.68 5.06 2.60 0.02 –0.01 0.05 0.05 –0.04 –0.08 –0.07
80 2.09 2.12 1.63 4.86 2.57 Metal –0.14 0.13 0.05 –0.12 –0.14 0.19 0.16
84 2.13 2.20 1.68 4.82 2.65a –0.14 0.00 –0.11 –0.11 0.02 0.06 0.10
98 1.92 2.15 1.71 5.14 2.46 Metallic 0.01 –0.09 –0.02 0.10 0.01 –0.07 –0.07
SE average 0.08 0.05 0.06 0.09 0.06 –0.06 –0.11 –0.06 0.06 –0.08 0.00 –0.08
Salt –0.02 0.00 0.03 0.02 –0.02 –0.05 –0.02
Means without superscripts do not differ from any other. –0.05 –0.03 0.04 0.05 0.01 –0.03 –0.02
a,b
Within traits, means that do not share a superscript differ (P < 0.000325 Sour 0.00 –0.16 –0.01 0.19 0.00 –0.14 –0.14
–0.04 –0.05 0.02 0.06 –0.02 0.05 –0.05
after correction for multiple testing).
Residuals were from a model that included the significant fixed effects of
transfer], ¼ Nellore ¼ Angus ¼ Brahman ¼ Hereford [produced with
contemporary group, slaughter date, electrical stimulation status, and slaughter
natural matings]), feeding pen (3 to 9 pens depending upon the year
age, and animal as a random effect.
and season of birth), age in days as a linear covariate, and slaughter
|r| > 0.11 differ from 0 (P < 0.05).
date (from 4 to 9 levels depending upon the year and season of birth).
Electrical stimulation status (electrically stimulated or not) was the
assessed in a distinct set of analyses in which the random animal
effect of interest. Animal was a random effect in the mixed linear
component was not modeled, but the effect of family (17 levels) per
models used for analyses in ASReml 3.1 (Gilmour et al., 2009). Pedigree
project design was included as a fixed effect. These were conducted to
information included 2419 individuals.
characterize specific family differences for traits.

2.3.2. Modeling family

The effect of family (either full-sibling embryo transfer families or 2.3.3. Correlations with other important traits
half-sibling families; the same four sires had both family types) was Pearson correlation coefficients among unadjusted and residual trait

Table 6
Correlation coefficients of unadjusted (below diagonal) and residual (above diagonal) values for pairs of flavor traits.
Trait 1 2 3 4 5 6 7 8 9 10 11 12 13 14

Acid (1) 0.20 0.33 –0.12 0.13 0.13 –0.08 –0.15 0.04 –0.04 –0.34 0.39 –0.26 0.51
Bitter (2) 0.10 0.12 0.11 0.03 0.04 –0.15 –0.13 0.04 –0.05 –0.17 0.37 –0.08 0.35
Bloody/Serum (3) 0.33 0.06 –0.44 0.09 0.06 0.08 –0.30 –0.06 –0.13 –0.04 0.58 –0.17 0.43
Browned (4) –0.27 0.15 –0.41 –0.26 –0.24 0.05 0.48 0.10 0.02 –0.14 –0.27 –0.13 –0.29
Chemical (5) 0.12 0.04 0.08 –0.10 0.81 –0.08 –0.14 0.09 –0.10 –0.03 0.09 0.00 0.14
Chemical burn (6) 0.10 0.02 0.07 –0.03 0.59 –0.06 –0.09 0.10 –0.08 –0.07 0.09 0.02 0.16
Cooked beef fat (7) –0.03 –0.07 0.11 0.05 0.01 0.05 0.25 –0.07 0.09 0.15 –0.04 0.28 –0.12
Cooked beef lean (8) –0.24 –0.01 –0.34 0.46 –0.20 –0.13 0.23 0.07 0.12 –0.06 –0.39 0.08 –0.41
Grassy (9) 0.04 0.13 –0.14 –0.03 –0.03 –0.02 –0.07 –0.12 –0.03 –0.16 –0.13 –0.27 –0.13
Livery (10) –0.05 0.03 –0.09 0.07 –0.11 –0.10 0.01 0.05 –0.01 0.14 –0.12 0.18 –0.07
Metal (11) –0.15 –0.10 0.00 0.01 0.11 0.03 0.01 –0.05 0.02 0.01 –0.03 0.59 –0.22
Metallic (12) 0.39 0.30 0.64 –0.26 0.19 0.18 –0.03 –0.28 0.02 –0.17 –0.08 –0.01 0.57
Salt (13) –0.17 0.02 –0.04 0.24 0.04 0.03 0.25 0.33 –0.12 –0.01 0.18 –0.13 –0.08
Sour (14) 0.45 0.20 0.36 –0.26 0.20 0.22 –0.09 –0.26 0.00 –0.03 –0.11 0.48 –0.13

Residuals were from a model that included the significant fixed effects of contemporary group, slaughter date, electrical stimulation status, and slaughter age, and
animal as a random effect.
|r| > 0.11 differ from 0 (P < 0.05).

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D.G. Riley, et al. Livestock Science 233 (2020) 103943

Table 8
Correlation coefficients of unadjusted (first row for each trait) and residual values (second row) for flavors traits paired with carcass and palatability traits.
Trait Maturity Marbling score Quality grade Shear force Juiciness Tenderness Connective tissue Flavor intensity

Lean Overall Myofibrillar Overall

Acid –0.03 –0.04 –0.15 –0.17 –0.06 0.24 0.17 0.19 0.12 –0.01
0.01 0.01 –0.05 –0.06 –0.05 0.24 0.13 0.14 0.09 –0.09
Bitter 0.09 0.12 –0.12 –0.13 –0.05 –0.13 –0.05 –0.05 0.01 –0.03
–0.03 –0.04 –0.10 –0.13 –0.06 –0.09 –0.03 –0.03 0.03 0.10
Bloody/serum 0.07 0.08 –0.08 –0.08 –0.09 0.41 0.24 0.24 0.19 –0.16
0.01 0.02 –0.10 –0.07 –0.07 0.57 0.29 0.30 0.22 –0.10
Browned 0.05 0.06 0.12 0.11 0.21 –0.10 –0.18 –0.18 –0.18 0.40
0.07 0.04 0.04 0.04 0.06 –0.30 –0.23 –0.23 –0.17 0.34
Chemical 0.02 –0.05 –0.20 –0.21 0.03 0.11 –0.06 –0.04 –0.07 –0.10
0.03 0.01 –0.06 –0.07 0.10 –0.03 –0.07 –0.07 –0.06 –0.17
Chemical burn 0.01 –0.06 –0.21 –0.21 –0.01 0.12 –0.03 –0.02 –0.06 –0.10
0.03 0.02 –0.01 0.00 0.04 –0.01 –0.07 –0.07 –0.08 –0.19
Cooked beef fat –0.10 –0.08 0.24 0.25 –0.12 0.19 0.18 0.18 0.16 0.24
–0.11 –0.09 0.06 0.10 –0.19 0.25 0.23 0.22 0.22 0.21
Cooked beef lean –0.15 –0.16 0.18 0.17 –0.02 0.15 0.16 0.15 0.13 0.75
–0.02 –0.02 0.11 0.12 –0.14 –0.04 0.15 0.14 0.20 0.65
Grassy –0.06 –0.04 –0.03 –0.05 0.08 0.12 –0.02 –0.01 –0.06 0.11
0.03 0.04 –0.01 –0.02 –0.01 –0.08 –0.07 –0.06 –0.04 –0.06
Livery –0.04 –0.06 0.03 0.04 –0.13 –0.10 0.10 0.09 0.09 0.13
0.00 0.00 0.07 0.05 –0.11 –0.10 0.08 0.08 0.09 0.11
Metal –0.05 –0.11 –0.02 –0.01 –0.08 –0.22 –0.05 –0.06 –0.01 –0.08
–0.02 –0.04 –0.04 –0.05 –0.05 –0.05 0.03 0.03 –0.01 0.04
Metallic 0.10 0.09 –0.15 –0.14 –0.03 0.15 0.04 0.05 0.03 –0.23
0.05 0.04 –0.09 –0.07 0.03 0.33 0.09 0.09 0.04 –0.12
Salt –0.08 –0.12 –0.07 –0.05 –0.14 –0.29 0.02 0.00 0.09 –0.04
–0.07 –0.08 0.03 0.04 –0.06 –0.10 0.07 0.06 0.12 0.21
Sour 0.11 0.11 –0.12 –0.13 –0.09 0.04 0.09 0.10 0.10 –0.25
0.03 0.01 –0.06 –0.06 –0.01 0.20 0.11 0.12 0.09 –0.09

Residuals were from a model that included the significant fixed effects of contemporary group, slaughter date, electrical stimulation status, and slaughter age, and
animal as a random effect.
|r| > 0.11 differ from 0 (P < 0.05).

values were used to assess correspondence of these traits 3. Results and discussion

1) with each other, within and across electrical stimulation status,
2) with the carcass and palatability traits in the companion reports,
and
3) with steer temperament measures at one year of age (aggressiveness,
gregariousness, flightiness, nervousness, and overall temperament;
Riley et al., 2014), and overall temperament as measured just prior
to slaughter.
2.3.4. Genome-wide association
Genotypes were from the Infinium BovineSNP50v1 chip assay
(Illumina, Inc., San Diego, CA). Genotypes were edited out of the final set
when 10% or more of the steers had missing genotypes, minor allele
frequency was less than 0.05, or for SNP with genotype frequencies that
deviated from Hardy-Weinberg proportions (P < 0.0001;
Wigginton et al., 2005). There were 34,957 SNP loci included in asso-
ciation analyses. The Q-K procedures of JMP Genomics (SAS Inst. Inc.,
Cary, NC) were used to conduct these mixed model analyses; genomic
relatedness was modeled with the SNP genotypes. Fixed effects were
determined as described in Section 2.3.1. A fixed regression on genotype
at each locus (covariate values of 0, 1, or 2 as the number of minor
alleles) was included as the test for association. Each trait measured on
each carcass side, corresponding to treatment (electrical stimulation) and
control, were considered distinct traits and sets of data; genome-wide
association analyses were conducted on each separately. Significant as-
sociations of loci with traits were declared with false discovery rate (FDR;
Benjamini and Hochberg, 1995) controlled at P < 0.05.
Nearest genes to each associated SNP locus were considered can-
didate genes and were identified using bovine reference genome as-
sembly UMD_3.1 (Zimin et al., 2009) and procedures of
Hulsman et al. (2014).
3.1. Fixed effects
Fifteen traits had very low means (< 0.02) and low numbers of non-
zero scores (< 23) measured either on steaks from sides with or
without electrical stimulation (Tables 2 and 3). These included the
flavors burnt, cardboard, cowy, dirt, fishy, milky, musty, nutty, old,
serum/broth, smoke, soapy, soda, soured, and sweet. These traits were
not analyzed further.
Contemporary group (n = 32; 8 to 15 steers per group) was mod-
eled in final models as steers born in the same year, fed in a set of two or
three small pens, and slaughtered on the same day. This was a sig-
nificant fixed effect in analyses of all flavor traits. Age at slaughter
approached significance (P = 0.07; 0.0008 ± 0.0004) for the flavor
livery, but was otherwise not important (P > 0.16). Samples from
electrically stimulated sides had greater (more intense) values of
cooked beef lean, livery, and acid flavors than samples from non-elec-
trically stimulated sides (P < 0.03; Table 4). However, samples from
non-electrically stimulated sides had greater (more intense) values for
browned flavor than samples from electrically stimulated sides. Elec-
trical stimulation status approached statistical significance (P = 0.084)
for the flavor bitter; otherwise this effect was not detected (P > 0.12).
3.2. Family as evaluated fixed effect
Family as a fixed effect was not important (P > 0.15) for the ma-
jority of the flavor traits evaluated. It was significant in analyses of
cooked beef lean, bitter, metal, and acid flavors (P < 0.03), and ap-
proached significance for cooked beef fat flavor (P = 0.06). After
correction for multiple comparisons, statistically significant differences
were only noted for a pair of families in the analyses of metal and acid
flavors (a distinct pair of families for each trait; Table 5).

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D.G. Riley, et al. Livestock Science 233 (2020) 103943

Table 9 single time per carcass. Those in Table 8 include more traditional
Correlation coefficients (r) of unadjusted (first row for each trait) and residual sensory panel traits and were measured on both carcass sides and
(second row) values of flavor traits with steer temperament at one year of age. therefore represent values unique to electrical stimulation status. Most
Trait A N F G O S of the correlation coefficients of flavor traits with carcass or palatability
traits (Table 8) were of low magnitude. Exceptions included flavor in-
Acid 0.00 –0.07 –0.08 0.07 –0.05 0.01 tensity with browned (r = 0.4 and 0.34 for unadjusted and residual
0.04 –0.02 –0.03 –0.04 0.00 0.03
values) and cooked beef lean (r = 0.75 and 0.65, for unadjusted and
Bitter –0.01 –0.01 –0.03 0.03 0.01 –0.06
–0.01 0.00 –0.02 0.05 0.03 –0.05 residual values), and juiciness with bloody/serum (r > 0.4).
Bloody/serum 0.11 0.05 0.04 0.09 0.08 –0.03 The correlation coefficients in Table 9 indicated minimal corre-
0.10 0.02 0.01 0.01 0.05 –0.05 spondence of either unadjusted or residual values of flavor traits with
Browned –0.06 –0.23 –0.22 –0.07 –0.21 –0.03
temperament traits measured at one year of age or immediately prior to
–0.05 –0.09 –0.08 –0.06 –0.09 0.02
Chemical –0.06 0.17 0.16 0.13 0.10 0.08
slaughter.
–0.01 0.11 0.11 0.09 0.11 0.01
Chemical burn –0.04 0.14 0.14 0.12 0.07 0.03 3.4. Genome-wide association
0.03 0.06 0.08 0.05 0.07 0.00
Cooked beef fat 0.00 0.02 0.06 0.11 0.04 0.10
From analyses of traits measured on steaks from carcass sides that
0.04 0.07 0.10 0.01 0.08 0.10
Cooked beef lean –0.15 –0.14 –0.12 0.00 –0.15 –0.09 were not subjected to electrical stimulation, two markers were asso-
–0.12 –0.15 –0.15 –0.13 –0.15 –0.15 ciated with cooked beef lean (one each on BTA 4 and 12), and one SNP
Grassy 0.01 –0.05 –0.05 0.05 –0.07 0.04 with sour on BTA 14 (Table 10). Relaxation of FDR to a maximum of
0.07 0.01 0.01 0.02 0.03 –0.01
0.17 (suggestive association: 0.05 < FDR < 0.17) resulted in an ad-
Livery –0.06 –0.03 –0.02 –0.01 –0.01 –0.14
–0.04 0.02 0.02 –0.02 0.01 –0.11
ditional 15 SNP of interest in analyses of chemical burn, cooked beef
Metal 0.01 0.10 0.11 –0.04 0.12 0.07 lean, livery, and sour flavors.
0.00 0.06 0.07 0.02 0.06 0.03 There were 4 SNP associated with acid (two markers), cooked beef
Metallic –0.01 0.08 0.07 0.12 0.12 0.01 lean, and metallic flavors assessed on steaks from sides exposed to
–0.02 0.13 0.12 0.09 0.14 0.01
electrical stimulation (Table 10). When FDR was permitted to be as
Salt –0.02 –0.09 –0.07 –0.07 –0.06 –0.12
–0.02 –0.07 –0.06 –0.07 –0.04 –0.11 high as 0.17, an additional 4 SNP had suggestive association with acid,
Sour 0.03 0.01 –0.01 0.09 0.02 –0.04 chemical burn, and cooked beef lean.
0.05 0.03 0.01 0.02 0.01 –0.03 There have been few reported results of similar analyses of flavor or
related traits. Sensory traits were evaluated on 8-point scales for grilled
Correlation coefficients of unadjusted and residual values are shown in the first
longissimus steaks from Charolais-Holstein cross steers (Gutiérrez-
and second rows corresponding to each in rows. Residuals for traits were from
Gil et al., 2008). That work reported QTL on BTA 7, 12, and 14 for
models that included fixed effects of contemporary group, slaughter date,
treatment (for traits measured that were subject to treatment), age, and animal assessment of the intensity of beef flavor and BTA 10 for the intensity of
as a random effect. beef odor. Those authors reported QTL for abnormal beef flavor (BTA
All scores were assigned from 1 to 9, with larger values representing unfavor- 14, 18, and 28) and abnormal beef odor (BTA 11 and 16). Gutiérrez-
able temperament; variables were averages of 4 evaluators (D.G. Riley et al., Gil et al. (2008) reported QTL for the same traits measured on roasted
2016). A = aggressiveness as the willingness of the animal to hit an evaluator. biceps femoris muscle, including beef flavor (BTA 22), beef odor (BTA
N = nervousness assessed by visual indications to include trembling, vocali- 25), abnormal beef flavor (BTA 29) and abnormal beef odor (BTA 12,
zation, and other activities (such as urination, etc.). F = flightiness indicated by 13, and 22). Gill et al. (2009) reported significant association of a single
running, jumping, or climbing behavior, gregariousness was the willingness and SNP within the gene growth hormone receptor on BTA 20 with a similar
comfort associated with being isolated from other animals. O = overall tem-
beef odor trait in Angus crossbred steers. Dang et al. (2014) evaluated
perament as a distinct assessment based upon all information observed.
“flavor likeness” as a 10-point attribute (1 = dislike extremely;
Slaughter temperament (S) was an assessment of all general aspects of tem-
10 = like extremely) averaged responses from a trained panel (7 to 9
perament by a single evaluator immediately prior to slaughter.
| r| > 0.11 differ from 0 (P < 0.05). panelists) in steaks from Hanwoo cattle. Those authors reported 6 as-
sociated SNP with this trait on BTA 4, 6 (approximately 3 Mb from one
3.3. Correlations of traits SNP in the present study with suggestive association with chemical
burn), 7, 23, 25, and 28.
The largest correlation coefficient among flavor traits was that for
chemical with chemical burn and metal with salt (r>0.58, Table 6). 3.4.1. Candidate genes—no electrical stimulation
The other strongest positive correlations of either unadjusted or re- Genes that were physically closest to each locus with significant
sidual values were browned with cooked beef lean, and pairs of these association are presented by electrical stimulation status in Table 10. A
flavor traits: acid, bloody/serum, metallic, and sour. Frank et al. (2016) gene on BTA 6 corresponded to chemical burn on steaks from sides with
reported similar positive values for correlations of flavors they termed no electrical stimulation—the marker was located within the gene
bloody, metallic, and sour/acidic flavors of beef. Additionally, boundaries. The protein NBCe1 is the product of solute carrier family 4
Miller et al. (2019) showed that beef identity and brown/roasted were member 4 (SLC4A4). This is a molecular transporter, especially involved
closely related and that bloody/serumy and sour were clustered when in reabsorption of renal bicarbonate (Romero et al., 1997).
beef steaks were evaluated using principal component analysis. Similar Closest genes to SNP associated with the cooked beef lean flavor on
results were reported by Luckemeyer (2015), Laird (2015) and steaks from sides without electrical stimulation were V-set and trans-
Glascock (2014). The largest negative relationships of unadjusted or membrane domain containing 2A (VSTM2A) on BTA 4 and neurobeachin
residual values were evidenced by correlation coefficients of bloody/ (NBEA) on BTA 12. V-set and transmembrane domain containing 2A is
serumy with browned (r = –0.41 and –0.44, respectively), and with involved in adipogenesis (Secco et al., 2017). The product of NBEA is
cooked beef lean (r = –0.34 and –0.3, respectively). Miller et al. (2019) integral for dendrite proliferation and formation of the electrical and
reported negative relationships for bloody/serumy with browned and chemical synapses of neurons in muscle (Su et al., 2004; Miller et al.,
beef identity. 2015); other BTA 12 SNP with suggestive association with this trait
Mostly weak relationships were observed of flavor traits with the included doublecortin like kinase 1 (DCLK1) and dachshund family tran-
traits in Tables 7 and 8. The carcass traits in Table 7 were measured a scription factor 1 (DACH1). The gene DLCK1 is also involved in neuronal
development, especially during mitosis (Shu et al., 2006;

5
D.G. Riley, et al. Livestock Science 233 (2020) 103943

Table 10
Markers with detected associations with flavor lexicon traits by electrical stimulation status.
Marker BTA Location (Mb) Trait Candidate gene Distance, bp

No electrical stimulation

FDR ≤ 0.05

rs109394766 4 0.87 Cooked beef lean V-set and transmembrane domain containing 2A (VSTM2A) 438,190
rs109578571 12 25.75 Cooked beef lean neurobeachin (NBEA) 44,850d
rs43705624 14 71.88 Sour dpy-19 like 4 (DPY19L4)
0.05 ≤ FDR ≤ 0.17

rs110251324 2 124.50 Chemical burn LOC100850739 162,642

rs42759118 6 10.18 Chemical burn peroxiredoxin-6 pseudogene (LOC784039) 46,924d
rs41605941 6 70.93 Chemical burn LOC100850829 83,145d
rs29016956 6 71.58 Chemical burn oligosaccharyltransferase complex subunit OSTC pseudogene (LOC100296974) 117,131
rs41588981 6 88.24 Chemical burn solute carrier family 4 member 4 (SLC4A4) 0
rs29024603 1 138.14 Cooked beef lean copine 4 (CPNE4) 0
rs110383845 1 148.68 Cooked beef lean RUNX family transcription factor 1 (RUNX1) 0
rs110532393 1 151.13 Cooked beef lean tetratricopeptide repeat domain 3 (TTC3) 0
rs42746341 1 157.46 Cooked beef lean LOC100848613 0
rs110054315 12 25.78 Cooked beef lean doublecortin like kinase 1 (DCLK1) 134,130
rs43699706 12 47.27 Cooked beef lean dachshund family transcription factor 1 (DACH1) 410,472
rs42194017 29 40.76 Cooked beef lean G protein subunit gamma 3 (GNG3) 427
rs42917200 2 114.06 Livery dedicator of cytokinesis 10 (DOCK10) 169,079
rs42805646 2 114.11 Livery dedicator of cytokinesis 10 (DOCK10) 221,011
rs110244995 29 46.10 Sour T-box 10 (TBX10) 28,310d
Electrical stimulation

FDR ≤ 0.05

rs110747179 16 49.73 Acid translocase of inner mitochondrial membrane 17A (TIMM17A) 60,181
rs109429155 23 40.53 Acid LOC100850899 44,030d
rs41599511 5 3.18 Cooked beef lean thyrotropin releasing hormone degrading enzyme (TRHDE) 827,189
rs43666745 11 15.81 Metallic latent transforming growth factor beta binding protein 1 (LTBP1) 0
0.05 ≤ FDR ≤ 0.17

rs42160968 29 2.14 Acid FAT atypical cadherin 3 (FAT3) 0

rs42444189 3 60.57 Chemical burn tubulin tyrosine ligase like 7 (TTLL7) 121,086
rs43708481 5 1.85 Cooked beef lean LOC100851721 40,880d
rs41634015 5 3.34 Cooked beef lean ataxin 7 like 3B (ATXN7L3B) 712,184d

Mb = chromosomal coordinates UMD_3.1 reference assembly (Zimin et al., 2009).

Minor allele frequencies ranged from 0.055 to 0.485.
Distance indicates the bp between the marker and the nearest candidate gene boundary. Values of 0 indicate markers within gene boundaries. Superscript d indicates
genes distal to markers and absence of that superscripts indicates genes centromeric to markers.

Fitzsimons et al., 2008). DACH1 was also the closest gene to SNP de-
tected as associated with marbling score in the present study, and has
been reported to be a component of products influential on embryonic
limb development (Kida et al., 2004). Among the SNP with suggestive
association with cooked beef lean (no electrical stimulation) were co-
pine 4 (CPNE4), RUNX family transcription factor 1 (RUNX1), and tetra-
tricopeptide repeat domain 3 (TTC3) on BTA 1 (all SNP were located
within the genes); and G protein subunit gamma 3 (GNG3) on BTA 29.
The lipopeptide produced by CPNE1 provides structural support during
cell membrane fusion and other cell life activities (Koukalová et al.,
2018). Transcription factors from the RUNX family, especially RUNX1,
also known as Cbfa1, are fundamental parts of expressed groups of
genes critical for progression of hematopoietic and osteogenic cell
lineages (Tracey and Speck, 2000; Karsenty, 2000; Woolf et al., 2003).
The first intron of GNG3 has a sequence element that is consensus with
RUNX1. These two genes, closest to two SNP suggestively associated
with cooked beef lean flavor, have a demonstrated regulatory interac-
tion in mouse T cell immune response (Dubeykovskiy et al., 2006). The
gene tetratricopeptide repeat domain 3 in humans is in the Downs syn-
drome critical region on HSA 21—it is one of several genes whose
duplication results in Downs syndrome. The protein TTC3 interacts
with other gene products in neuron development and differentiation
(Berto et al., 2007; Kim et al., 2019).
A SNP associated with the flavor sour was closest to the gene dpy-19
like 4 (DPY19L4) on BTA 14. Proteins in the Dpy19L family appear to be
involved in cell structural organization (Watanabe et al., 2016). This
gene produces a protein involved in neuron development that facilitates
growth of axons or dendrites (Shcherbakova et al., 2017). On BTA 29, a
locus at 46.1 Mb (in the same region of BTA 29 as detected associations
with tenderness) with suggestive association with the flavor sour (no
electrical stimulation) was closest to T-box 10 (TBX10). The T-box fa-
mily of genes are conserved across many species and are contributors to
vertebrate developmental processes (Law et al., 1998; Naiche et al.,
2005); alterations or mutations of these genes often have severe con-
sequences from a development and fitness standpoint (Kojima et al.,
2013). Two BTA 2 SNP suggestively associated with livery flavor were
closest to dedicator of cytokinesis 10 (DOCK10), which has documented
roles in immunological activities (Yelo et al., 2008; Ruiz-Lafuente et al.,
2019) and neural development (Jaudon et al., 2015).
3.4.2. Candidate genes—electrical stimulation
The closest genes to SNP with suggestive or significant association
with acid flavor in steaks from electrically stimulated sides were FAT
atypical cadherin 3 (FAT3) on BTA 16 (the marker was within gene
boundaries) and translocase of inner mitochondrial membrane 17A
(TIMM17A) on BTA 29. FAT atypical cadherin 3 encodes a protein
component of a tissue development signaling module within neuronal
growth and assembly (Deans et al., 2011; Saburi et al., 2012). There are
channels in the inner membrane of mitochondria supported by a
complex that transports proteins from the nucleus to the mitochondria;

6
D.G. Riley, et al.
TIMM17A is a subunit affiliated with the membrane and part of this
complex (Moro et al., 1999; Wang et al., 2012).
Two genes on BTA 5 were closest to SNP with at least suggestive
association with the flavor cooked beef lean in steaks from carcass sides
subjected to electrical stimulation: thyrotropin releasing hormone de-
grading enzyme (TRHDE) and ataxin 7 like 3B (ATXN7L3B). The gene
TRHDE has been identified as a candidate for various production traits
in small ruminants, including post weaning gain in a research popula-
tion of Chinese Sunit and German Mutton sheep (Zhang et al., 2013;
Zhang. 2016), internal fat amount in Merino sheep (Cavanagh et al.,
2010), fatty acid profiles in Santa Inês sheep (Rovadoscki et al., 2018),
and was reported with evidence of selection in North African popula-
tions of goats (Kim et al., 2015). The gene ATXN7L3B produces a pro-
tein involved in histone development and related structural compo-
nents (Li et al., 2016).
The SNP on BTA 11 significantly associated with the flavor metallic
was within the boundaries of the gene latent transforming growth factor
beta binding protein 1 (LTBP1) which is a protein component of extra-
cellular matrix microfibrils (Isogai et al., 2003). The closest gene to a
marker (suggestively) associated with chemical burn flavor on BTA 3
(tubulin tyrosine ligase like 7; TTLL7) produces a functional and organi-
zational component of tubules in neurons (Mukai et al., 2009;
Garnham et al., 2015).
4. Conclusions
Half (n = 15) of the 30 flavor traits evaluated in this work lacked
variation for any type of analysis. Electrical stimulation status was in-
fluential in only 5 of the 15 flavor traits evaluated: more intense acid,
bitter, and browned flavors were noted after no electrical stimulation;
more intense cooked beef lean and livery flavors were detected for
steaks from carcass sides that were electrically stimulated. Few corre-
lation coefficients of large magnitude were detected for these flavor
traits with other carcass or palatability traits. There were no strong
correspondences of flavor traits with steer temperament at one year of
age or immediately prior to slaughter. There were a small number of
SNP with association to flavor traits when FDR < 0.18. Many of the
closest genes to those SNP had relationship to neural development or to
structure of various tissues.
Funding
This project was supported in part by National Research Initiative
Competitive Grant no. 2008–35205–18,767 from the USDA National
Institute of Food and Agriculture; by beef and veal producers and im-
porters through their $1-per-head checkoff; and by Texas A&M AgriLife
Research.
Declaration of Competing Interest
None.
Acknowledgements
Appreciation is noted for R. R. Riley and all personnel at the Texas
A&M University Rosenthal Meat Science and Technology Center in
College Station, and B. D. Johnson, M. D. Freedman, and all personnel
at the Texas A&M AgriLife Research Center at McGregor.
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