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. 2021 Feb 6;99(2):skab039. doi: 10.1093/jas/skab039

The Blonde d’Aquitaine T3811>G3811 mutation in the myostatin gene: association with growth, carcass, and muscle phenotypes in veal calves

Aurélie Vinet 1, Claire Bouyer 2, Lionel Forestier 2, Ahmad Oulmouden 2, Véronique Blanquet 2, Brigitte Picard 3, Isabelle Cassar-Malek 3, Muriel Bonnet 3, Dominique Rocha 1, Gilles Renand 1,✉
PMCID: PMC7904057  PMID: 33624102

Abstract

The mutation T3811 → G3811 (TG3811) discovered in the myostatin gene of the Blonde d’Aquitaine breed is suspected of contributing to the outstanding muscularity of this breed. An experiment was designed to estimate the effect of this mutation in an F2 and back-cross Blonde d’Aquitaine × Holstein population. By genotyping all known mutations in the myostatin gene, it was ensured that the TG3811 mutation was indeed the only known mutation segregating in this population. Fifty-six calves (43 F2, 13 back-cross) were intensively fattened and slaughtered at 24.0 ± 1.4 wk of age. The effects of the mutation were estimated by comparing the calves with the [T/T] (n = 18), [T/G] (n = 30), and [G/G] (n = 8) genotypes. Highly significant substitution effects (P < 0.001), above + 1.2 phenotypic SD, were shown on carcass yield and muscularity scores. Birth weight (P < 0.001) was positively affected by the mutation (+0.8 SD) but not growth rate (P = 0.97), while carcass length (P = 0.03), and fatness (P ≤ 0.03) were negatively affected (–0.5 to –0.7 SD). The characteristics of the Triceps brachii muscle were affected by the mutation (P < 0.001), with lower ICDH activity (oxidative) and a higher proportion of myosin type 2X muscle fibers (fast twitch). The effects of the TG3811 mutation were similar to those of other known myostatin mutations, although the Blonde d’Aquitaine animals, which are predominantly [G/G] homozygous, do not exhibit extreme double muscling.

Keywords: beef cattle, carcass, muscle, myostatin

Introduction

The growth differentiation factor 8 gene (GDF8), generally known as myostatin gene, was shown to be responsible for muscle hypertrophy of the colloquially termed double-muscled cattle when animals carry 2 copies of disruptive mutations in this gene (Grobet et al., 1997; Kambadur et al., 1997; McPherron and Lee, 1997). These authors found 2 disruptive mutations in the third exon: the nt821 mutation (11-bp deletion) truncates the bioactive part of the protein and was found in Belgian Blue double-muscled animals; the C313Y mutation (G → A transversion), found in Piedmontese double-muscled animals, changes a cysteine to tyrosine in the bioactive part of the protein and consequently results an almost complete loss of function. Additional mutations have been found in the coding regions of the myostatin gene of Bos taurus cattle (Cappucio et al., 1998, Grobet et al., 1998; Dunner et al., 2003). Some mutations were predicted to be disruptive as a consequence of a premature stop codon: Q204X, nt419, and E226X in the second exon of Charolais or Maine-Anjou double-muscled animals and E291X in the third exon of double-muscled Marchigiana animals. In addition to these disruptive mutations, responsible of double-muscling, a G → A transversion, was revealed in the first exon resulting in a substitution of leucine for phenylalanine at amino acid position 94. This missense mutation (F94L) was predominantly found in well muscled but not double-muscled Limousin cattle. This mutation (F94L) is unlikely to cause the loss of the function of the gene but has nevertheless been found to be associated with an increase in muscularity compared with the wild-type allele (Sellick et al., 2007; Esmailizadeh et al., 2008). In addition to these mutations in coding regions, a single-nucleotide polymorphism (SNP; TG3811), a T → G transversion (BTA2 g.6,282,805, ARS-UCD1.2 assembly), was discovered in the second intron of the myostatin gene of Blonde d’Aquitaine cattle and this polymorphism was shown to be responsible of an aberrant transcript (Bouyer et al., 2014). Among 445 animals of 24 different breeds, this SNP was only found in the Blonde d’Aquitaine breed. It was almost fixed in this breed whose animals exhibit outstanding muscularity but no muscular hypertrophy as observed in extreme double-muscled cattle. This unexpected mutation was suspected to contribute to the remarkable muscularity of the Blonde d’Aquitaine animals (Bouyer et al., 2014).

The objective of the present study was to verify and quantify the impact of the TG3811 polymorphism found in Blonde d’Aquitaine on growth, carcass and muscle phenotypes of beef calves in a Blonde d’Aquitaine x Holstein crossbred population segregating this polymorphism.

Materials and Methods

During this experiment, all animals were handled with care, following the INRAE ethics policy in accordance with the guidelines for animal research issued by the French Ministry of Agriculture (Légifrance, 2013).

Animals and management

For this study, an experimental population was specially designed by mating homozygotes [G/G] Blonde d’Aquitaine bulls to Holstein cows, presumably homozygotes wild type [T/T] in order to observe the segregation of the TG3811 polymorphism and to quantify the effect of the mutation on beef traits. Three Blonde d’Aquitaine bulls were mated by artificial insemination (AI) to Holstein cows in commercial herds in order to procreate F1 crossbred progeny. About 30 F1 male and female calves were entered the AI center from AURIVA Cooperative (Soual, France). Three F1 male calves, 1 per Blonde d’Aquitaine sire, were used to inseminate either F1 females, in order to produce F2 embryos, or Holstein cows, in order to procreate back-cross (BC) progeny. After puberty, 10 F1 female calves were super-ovulated and inseminated with F1 bull semen. After quality control, the F2 embryos were frozen in liquid nitrogen.

In the INRAE experimental farm at Carmaux, Aubrac beef heifers were used as recipients for the embryo transfers. A total of 45 F2 and 13 BC calves were born over a 14-wk period and dispatched in 5 fattening batches according to their date of birth. After calves were fed their dam’s colostrum, they were separated from their dam and moved to a nursery where they received an automatically distributed milk diet. The milk composition was about 60% skim milk powder, supplemented with palm and canola oil, whey powder, starch, and lactose. The quantity of milk available was gradually increased until the calves were fed ad libitum from 2 months of age. During the last 14 wk they consumed daily around 2.5 ± 0.3 kg dry matter on average. Eventually, they were slaughtered at 24.0 ± 1.4 wk of age.

DNA extraction and SNP genotyping

Blood samples of calves and F1 dams were collected by jugular venipuncture. DNA was extracted from 200 µL of fresh blood using the QIAamp DNA Blood Mini QIAcubekit (Qiagen) according to the manufacturer’s instructions. DNA quantity and quality were measured using a Nanodrop (Thermo Scientific). DNA samples were then stored at −20 °C until use. The TG3811 polymorphism was determined using PCR-RFLP approach (Bouyer et al., 2014). A 763-bp fragment encompassing the SNP was amplified by PCR from genomic DNA, digested with AflII restriction enzyme (New England Biolabs) and size fractionated by agarose gel electrophoresis. The G3811 allele for the TG3811 polymorphism removes the restriction site that cleaves the wild-type T3811 allele into 565- and 198-bp fragments.

The genotype of the 3 Blonde d’Aquitaine and the 3 F1 sires was determined from their semen DNA. They were genotyped for the TG3811 polymorphism and 8 mutations known to affect the coding sequence in the main breeds of beef cattle (Miranda et al., 2002): 6 disruptive mutations (nt419, Q204X, E226X, nt821, E291X, and C313Y) and 2 missense mutations (F94L and S105C).

Phenotypes

Birth weight was recorded for all the BC and F2 calves, while gestation length was available only for F2 calves. Calves were weighed every 2 wk, and average daily gain was calculated between birth and final fattening weights. The last day of fattening the calves were visually scored on a 15-point scale for the following phenotypes: muscularity (1 = poorly muscled; 15 = extremely muscled); fatness (1 = extremely lean; 15 = extremely fat); cannon bone thinness (1 = very thick; 15 = very thin). The thinness of the skin was evaluated by manipulation and scored on a 15-point scale (1 = very thick; 15 = very thin). At slaughter the hot carcass was weighted and the dressing percentage calculated in relation to the final body weight. The next day, the following linear phenotypes were measured: the length of the carcass from the pubic symphysis to the edge of the first rib; the length of the leg from the pubic symphysis to the articular surface of the metatarsus; the maximum width of the thigh (De Boer et al., 1974). The carcasses were scored for the following phenotypes: muscularity (1 = poorly muscled; 15 = extremely muscled); cover fatness (1 = extremely lean; 15 = extremely fat); internal fatness (1 = extremely lean; 15 = extremely fat); muscle redness (1 = light pink; 5 = intense red). Twenty-four hours after slaughter, samples of Longissimus thoracis (LT) muscle, Triceps brachii (TB) muscle and kidney fat were excised from the carcass at the same place for all cattle. The lateral part of the TB muscle was collected, and the LT muscle was sampled in the middle of the 6th rib cut. An average of 150 g were collected, stored at –80 °C and powdered in liquid nitrogen before analysis. The oxidative metabolism was quantified by the measurement of the isocitrate dehydrogenase (ICDH) activity (Briand et al., 1981). The anaerobic glycolytic metabolism was quantified by the measurement of the lactate dehydrogenase (LDH) activity (Ansay, 1974). The muscle contractile type was quantified by the proportion of type I, 2A, and 2X myosin heavy chains measured by electrophoresis (Picard et al., 2011).

Statistical analysis

First, a model was applied to remove factors known to influence carcass and growth phenotypes: 2 subpopulations (F2 or BC), 3 sire families; 2 sex (male or female), and 5 fattening batches. The residual variance of the first model was an estimate of the phenotypic variability. The effect of the 3 genotypes ([T/T], [T/G], and [G/G]) was estimated in a second model, in addition to the former factors, using the GLM procedure of the SAS/STAT software (SAS Institute, 2018). The T → G allele substitution effect was estimated in a third model, with the same main factors and a regression on the number of G allele copies: 0, 1, or 2 copies, respectively, for [T/T], [T/G], and [G/G] animals. The substitution effect was divided by the phenotypic standard deviation (SD) for a standardized comparison of the TG3811 effects across the different phenotypes.

Results

The performances of 2 outlier animals, out of the 58 recorded, were discarded from analysis due to health problems. Summary statistics are reported in Table 1. The analysis of variance showed that, among the different base model factors, differences between the 5 fattening batches were the most important and affected most traits. The sex of the calf was significant only on birth weight and fatness scores, with lower birth weight and higher fatness for female calves. The muscularity of BC calves was significantly lower compared with F2 calves. There was no difference between the 3 sire families for all traits.

Table 1.

Statistics of the recorded traits

Trait1 Unit n Mean RSD2
Live animal
Gestation length d 43 279.0 3.3
Birth weight kg 56 42.9 3.7
Average daily gain
 kg/d
 56
1.20
0.09
Final age d 56 169 5
Final weight kg 56 227 16
Muscularity score /15 56 7.34 1.32
Fatness score /15 56 7.36 1.68
Bone thinness score /15 56 7.79 1.08
Skin thinness score /15 56 7.36 2.16
Carcass
Dressing percentage /100 56 56.7 2.2
Hot carcass weight kg 56 129 11
Carcass length mm 56 1032 28
Leg length mm 56 685 13
Thigh width mm 56 204 11
Muscularity score /15 56 7.45 1.57
Cover fatness score /15 56 7.32 1.66
Internal fatness score /15 56 7.52 1.64
Redness score /5 56 3.16 0.76
LT muscle
ICDH µmol/min/g protein 54 7.96 2.06
LDH µmol/min/g protein 54 5157 500
Myosin type 1 /100 55 12.0 3.9
Myosin type 2A /100 55 34.2 10.4
Myosin type 2X /100 55 53.7 11.0
TB muscle
ICDH µmol/min/g protein 54 11.28 2.62
LDH µmol/min/g protein 54 5061 348
Myosin type 1 /100 56 14.5 3.5
Myosin type 2A /100 56 21.3 3.7
Myosin type 2X /100 56 64.2 5.7
Kidney fat
ICDH µmol/min/g protein 56 146 32
LDH µmol/min/g protein 56 1953 412
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1LT, longissimus thoracis; ICDH, isocitrate dehydrogenase; LDH, lactate dehydrogenase; TB, triceps brachii.

2RSD, residual (phenotypic) SD of traits adjusted for nongenetic effects.

The 3 Blonde d’Aquitaine first generation sires were homozygous [G/G] and the 3 F1 sires were heterozygous [T/G] for the TG3811 mutation. All the 6 sires were homozygous wild-type for other myostatin mutations. Among the 43 F2 calves, 25 were heterozygous [T/G], 10 homozygous [T/T], and 8 homozygous [G/G]. Among the 13 BC calves, 8 were [T/T] and 5 were [T/G]. In the 2 subpopulations frequencies did not deviate significantly from Hardy–Weinberg expectations (P = 0.52 and P = 0.27, respectively).

Results of the analysis of the genotype effects are reported in Table 2. The mutation had a significant effect on most live or carcass traits, except on growth traits and leg length. Comparison of genotype means shows that there was no significant dominance effect of the mutation on most traits except for dressing percentage and muscularity scores with a moderate recessive effect (data not shown). Muscularity scores of homozygous [G/G] calves were over 60% higher than those of wild-type [T/T] calves (P < 0.001). Birth weight (P = 0.001), dressing percentage (P < 0.001), carcass weight (P = 0.005), and thigh width (P < 0.001) of [G/G] calves were 12% higher on average than [T/T] calves. In contrast, the carcass muscle redness (P = 0.002) and carcass fatness scores (P = 0.001 and P = 0.02) of [G/G] calves were 30% lower on average than those of [T/T] calves. The cannon bone (P = 0.03) and skin (P < 0.001) of [G/G] calves were thinner, 20% and 50% respectively, compared with [T/T] calves. The muscle characteristics of the TB were significantly dependent of the genotype, while few relationships were observed for the LT characteristics. The TB muscle of [G/G] calves was more fast-glycolytic type with higher proportion of myosin type 2X (P < 0.001) and lower ICDH activity (P < 0.001) compared with [T/T] calves. A trend was observed for reduced LDH (P = 0.03) enzyme activity in the kidney fat of [G/G] and [T/G] calves relatively to the [T/T] calves.

Table 2.

Analyses of variance and estimates of genotype and substitution effects

Effect Genotype Least square means Substitution effect
Trait1 P-value [T/T] [T/G] [G/G] α 2 P-value
Live animal
Gestation length 0.08 277.8a 280.9b 280.6ab 0.46 0.09
Birth weight 0.004 43.2a 46.3b 48.9b 0.79 <0.001
Average daily gain 0.36 1.18 1.22 1.17 0.00 0.97
Final weight 0.57 231 237 234 0.14 0.57
Muscularity score <0.001 5.94a 7.07b 9.52c 1.27 <0.001
Fatness score <0.001 8.05a 6.32b 5.10b –0.91 <0.001
Bone thinness score 0.002 7.26a 7.23a 8.83b 0.60 0.02
Skin thinness score <0.001 8.24a 9.03a 12.36b 0.85 <0.001
Carcass
Dressing percentage <0.001 54.6a 56.0b 60.6c 1.25 <0.001
Hot carcass weight 0.02 126a 133ab 141b 0.67 0.004
Carcass length 0.03 1041a 1038a 1006b –0.53 0.03
Leg length 0.38 694 692 684 –0.31 0.21
Thigh width <0.001 198a 207b 225c 1.13 <0.001
Muscularity score <0.001 5.78a 6.99b 9.95c 1.23 <0.001
Cover fatness score 0.004 8.23a 7.45a 5.59b –0.74 0.002
Internal fatness score 0.06 8.13a 7.70a 6.21b –0.53 0.03
Redness score 0.002 3.71a 2.92b 2.54b –0.82 <0.001
LT muscle
ICDH 0.044 9.18a 7.62b 6.87b –0.59 0.02
LDH 0.78 4924 5036 4920 0.03 0.92
Myosin type 1 0.35 12.7 14.6 13.2 0.14 0.59
Myosin type 2A 0.19 40.5 40.5 32.1 –0.33 0.19
Myosin type 2X 0.14 46.8ab 44.8a 54.7b 0.27 0.29
TB muscle
ICDH <0.001 12.90a 10.19b 7.84c –0.97 <0.001
LDH 0.09 4923 5123 4826 –0.04 0.87
Myosin type 1 <0.001 15.7a 16.4a 11.4b –0.47 0.06
Myosin type 2A 0.006 25.4a 22.7b 19.5c –0.79 0.001
Myosin type 2X <0.001 58.9a 60.9a 69.0b 0.80 <0.001
Kidney fat
ICDH 0.12 149 126 124 –0.45 0.08
LDH 0.06 2034a 1674b 1724ab –0.46 0.07
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1LT, longissimus thoracis; ICDH, isocitrate dehydrogenase; LDH, lactate dehydrogenase; TB, triceps brachii.

2α is the slope of the regression of phenotypes on the number of TG3811 allele copies, divided by RSD.

a,b,cWithin a row, means without a common superscript letter differ (P < 0.05).

Discussion

The results show that the TG3811 mutation found in Blonde d’Aquitaine animals was significantly associated to beef trait differences between genotypes. All 3 F1 sires used in this experiment being [T/G] heterozygous for this mutation and homozygous for the wild-type allele of all other known mutations in the myostatin gene, the presence of 1 or 2 copies of the TG3811 mutation was most probably the unique origin of differences between the genotypes.

This mutation was shown to be responsible for an aberrant transcript and consequently for a truncated protein lacking the entire bioactive region (Bouyer et al., 2014). This mutation could be considered as a disruptive mutation therefore, similarly to other disruptive mutations found in exons of this gene. However, Bouyer et al. (2014) also observed some expression of normal transcript in homozygous [G/G] animals and speculated this mutation may not be entirely disruptive and may prevent extreme muscle hypertrophy. In the literature, there are studies with estimates of the effects of the different disruptive mutations on muscle hypertrophy (mh mutations) either in designed cross experiments or in commercial populations: C313Y (Short et al., 2002), nt811 (Casas et al., 2004; Gill et al., 2009; Wiener et al., 2009; Allais et al., 2010), Q204X (Allais et al., 2010), and E291X (Sarti et al., 2014). The effects of the nondisruptive F94L mutation were also estimated by Esmailizadeh et al. (2008), Alexander et al. (2009), and Cushman et al. (2015). The comparison of these estimates across studies is difficult because they are expressed in different units, either in gross value or as a proportion of phenotypic SD or as a percentage of trait means. However, the superiority of heterozygous [+/mh] over wild-type [+/+] animals and the superiority of 2 mutated copy carriers [mh/mh] over heterozygous [+/mh] animals can be calculated from results of the study by Short et al. (2002), Gill et al. (2009), Wiener et al. (2009), Allais et al. (2010), and Sarti et al. (2014) in populations in which was segregating one of the following mh mutations: C313Y, nt821, Q204X, or E291X. An average of 0.7 [0.4 to 1.4] and 2.0 [1.6 to 2.6] phenotypic SD can be calculated, respectively, for the 2 differences, ([+/mh] – [+/+]) and ([mh/mh] – [+/mh]), for muscle development traits (muscularity score, rib eye area, thigh or rump width, muscle weight or content). These values are very similar to the differences observed in the present study: 0.8 to 0.9 SD for the [T/G] superiority and 1.6 to 1.9 SD for the [G/G] superiority. The lower fatness of animals carrying 1 or 2 copies of the mutated allele in the mentioned studies for different fat-related traits (fatness score, fat depth, intern fat, rib fat, and fat content) is similar to the reduction of fatness found in this study. The ([+/mh] – [+/+]) differences average –0.5 [0.0 to –1.0] in the literature studies and –0.6 [–0.3 to –1.0] in the present study and the ([mh/mh] – [+/mh]) differences average –1.1 [–0.4 to -1.8] in the literature studies and –0.9 [–0.7 to –1.1] in the present study. Although no direct comparison can be drawn from these different studies, the results of the present study are in line with the published estimates for mh mutations. In contrast, the results of a Limousin × Jersey experiment show that the additive effects of the F94L mutation on muscle and fat phenotypes are markedly lower (Esmailizadeh et al., 2008). Although Bouyer et al. (2014) suggested that the TG3811 mutation was not entirely disruptive, the effects of TG3811 in the present study were very similar to the effects of disruptive mh mutations. A recent study on the herds of the Blonde d’Aquitaine nucleus in France showed that 97.5% of the 9,880 genotyped animals were [G/G] homozygous and 1.6% carried also an mh (nt419 or Q204X) mutation in addition to the TG3811 mutation (Renand et al., 2020). These double heterozygous calves ([G+/Tmh]) had a superior muscularity score at weaning (+0.36 SD) compared with homozygous [G+/G+] calves. These results show that the disruptive mh mutations actually have a higher effect on muscularity when compared with the TG3811 mutation.

The carcass higher muscularity and lower fatness of double-muscled cattle over normal cattle has been well documented for several decades, as has the impact on other production traits (Ménissier, 1982; Arthur, 1995). The birth weight of [G/G] homozygous calves was 13% higher than the birth weight of [T/T] calf, within the lower range of 10% to 30% discussed by Ménissier (1982), and similar to the 12% reported by Short et al. (2002) and Wiener et al. (2009) for the C313Y and nt821 mutation, respectively. The reduction in the size of the leg and the thickness of the cannon bone confirms previous observations cited by Arthur (1995) and results reported by Allais et al. (2010). The thinner skin of [G/G] calves is consistent with the results reported by Ménissier (1982) that the skin weight of double-muscled cattle was lower than that of normal cattle, possibly related to a lower synthesis of collagen as observed in the LT muscle of [+/mh] compared with [+/+] Charolais bulls (Allais et al., 2010).

Regarding the characteristics of the muscles, the same tendency is observed in both muscles although more marked in the TB muscle: a decrease in oxidative metabolism and in proportion of myosin 2A simultaneously with an increase in proportion of myosin 2X. This modification in the muscle characteristics toward orientation to more glycolytic metabolism is in agreement with the positive relationships between fast glycolytic properties and muscle mass, whatever its genetic origin, either monogenic (myostatin mutation) or polygenetic (for cattle selected for high muscle growth) (Bouley et al., 2005; Picard et al., 2005; Picard and Gagaoua, 2020). A fetal origin with a higher proliferation of the second generation of fibers at the origin of fast glycolytic fibers in adult was described in double-muscled fetuses (Duris et al., 1999; Gagnière et al., 2000; Deveaux et al., 2001) or Blonde d’Aquitaine fetuses (Cassar-Malek et al., 2017) compared with age-matched Charolais. The fiber-type composition is coherent with the paler color of muscle on the carcass of [G/G] calves as observed in double-muscled cattle (Fiems et al., 2012). The highest differences observed for TB comparatively to LT muscle are in agreement with the data of the literature, indicating that in double-muscled cattle, the LT is isotrophied as the TB was hypertrophied (Picard and Gagaoua, 2020).

Regarding the characteristics of adipose tissues, in addition to a reduced amount of fat, the observed trend for lower LDH and ICDH activities in the kidney fat of [G/G] and [T/G] than the [T/T] calves suggests that a lower lipogenic activity is associated with TG3811 mutation. Indeed, carbon from lactate and hydrogen provided by nicotinamide adenine dinucleotide phosphate (NADP)-linked dehydrogenases both contribute to fatty acids synthesis. Thus LDH, as the enzyme responsible for lactate production from glucose, and ICDH, as one of the NADP-linked dehydrogenases, may affect the lipogenic potential of adipose tissues in bovine (Vernon, 1980). Lower LDH and ICDH activities were repeatedly observed when lipogenic activities, adipose tissue cellularity, or body fatness were decreased (Pothoven and Beitz, 1973; Eguinoa et al., 2003; Zhang et al., 2012). Therefore, the TG3811 mutation most probably has a direct effect on lipid metabolism in addition to its marked effect on muscle fiber growth and differentiation.

Conclusion

The recently discovered TG3811 mutation in the second intron of the myostatin gene was found to be most probably responsible for significant carcass and muscle superiority. The present study also showed that these effects were similar to the effects of already known mh mutations such as the nt821, C313Y, or Q204X responsible for double muscling. This mutation is almost fixed in the Blonde d’Aquitaine breed in France. If animals of this breed have a superior muscularity, they do not exhibit extreme double muscling. Apparently, the expression of this mutation in purebred Blonde d’Aquitaine differs from that of other disruptive mh mutations. It would be very interesting to design an experiment, crossing double heterozygous [G+/Tmh] Blonde d’Aquitaine sires to Holstein cows in order to procreate F1 females and backcrossing these F1 females with these [G+/Tmh] Blonde d’Aquitaine sires. Such design will allow to compare the respective effects of the TG3811 and mh mutation, in the same population where both mutations will be segregating.

Glossary

Abbreviations

AI

artificial insemination

GDF8

growth differentiation factor 8 gene

mh

muscle hypertrophy

NADP

nicotinamide adenine dinucleotide phosphate

SNP

single-nucleotide polymorphism

Conflict of interest statement

The authors declare no real or perceived conflicts of interest.

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