Detection of an indel 20 bp polymorphism in the CDC25A gene of Saburai does (Capra hircus): a preliminary study

Detecção de um polimorfismo de inserção/deleção de 20 pb no gene CDC25A de cabras Saburai (Capra hircus): um estudo preliminar

Abstract

Cell division cycle 25A (CDC25A) is one of candidate genes to improve productivity traits of sheep. Many previous studies reported that this gene has a polymorphic site at the intron 9 region, namely indel 20 mutation. This study aimed to detect the indel 20 bp mutation in CDC25A gene of Saburai does (Capra hircus) and its association with growth traits i.e. birth weight, weaning weight, yearling weight and preweaned/postweaned daily weight gain. As a preliminary study, 24 female goats (does) from Tanggamus Regency were used in this study for the investigation. Results showed that the indel 20 bp mutation was observed in CDC25A gene of Saburai does. Three genotypes of DD (0.46), ID (0.37) and II (0.17) were identified in the indel 20 bp locus of Saburai CDC25A gene. Therefore, the polymorphic informative content (PIC) in this locus was 0.35 (high) and indicating a good parameter for a genetic marker. However, the polymorphism of indel 20 bp in caprine CDC25A gene was not significantly associated with growth traits of Saburai does. In conclusion, the polymorphism in the indel 20 bp locus of caprine CDC25A gene had the potency for a genetic marker of growth traits in Saburai goats.

Keywords:
CDC25A gene; growth traits; indel 20 bp mutation; polymorphism; Saburai goats

Resumo

O gene CDC25A (ciclo de divisão celular 25A) é um dos genes candidatos para melhorar características de produtividade em ovinos. Muitos estudos anteriores relataram que esse gene possui um sítio polimórfico na região do íntron 9, denominado mutação de inserção/deleção de 20 pb. Este estudo teve como objetivo detectar a mutação de inserção/deleção de 20 pb no gene CDC25A de cabras Saburai (Capra hircus) e sua associação com características de crescimento, como peso ao nascer, peso ao desmame, peso ao ano e ganho de peso diário pré e pós-desmame. Como estudo preliminar, 24 cabras fêmeas da região de Tanggamus foram utilizadas nessa investigação. Os resultados mostraram que a mutação de inserção/deleção de 20 pb foi observada no gene CDC25A das cabras Saburai. Três genótipos, DD (0,46), ID (0,37) e II (0,17), foram identificados no lócus de inserção/deleção de 20 pb do gene CDC25A da raça Saburai. Portanto, o conteúdo informativo polimórfico (PIC) neste lócus foi de 0,35 (alto), indicando um bom parâmetro para um marcador genético. No entanto, o polimorfismo da inserção/deleção de 20 pb no gene CDC25A caprino não apresentou associação significativa com as características de crescimento das cabras Saburai. Em conclusão, o polimorfismo no lócus de inserção/deleção de 20 pb do gene CDC25A caprino demonstrou potencial como marcador genético para características de crescimento em cabras Saburai.

Palavras-chave:
gene CDC25A; características de crescimento; mutação de inserção/deleção de 20 pb; polimorfismo; cabras Saburai

1. Introduction

Goats are the important livestock that kept for meat production purpose in Indonesia. In year 2024, the prediction of chevon production in Indonesia was about 95,361 tons and the prediction of chevon consumption in Indonesia at the same time was about 53,273 tons (Kementan RI, 2020). Hence, about 42,088 tons (55.86%) of chevon surplus production can be exported to other countries. Increasing of meat production can be assessed with a molecular selection program. Cell division cycle 25A (CDC25A) gene is one of candidate genes that used to improve the productivity traits in goats based on genome-wide association study (GWAS) analysis (Wang et al., 2016). The caprine CDC25A gene (GenBank: NC_030829.1) is located at 15^th chromosome along 22,061 bp with 15 exons. The CDC25A is a dual-specificity protein phosphatase that plays crucial role in cell cycle regulator for activating the apoptotic cell cycle pathway (Shen and Huang, 2012; Biswas et al., 2017). In addition, the CDC25A can regulates cell proliferation and axis extension during gastrulation in zebrafish (Liu et al., 2017) and ensuring the health and genomic stability during embryo development in mice (Lee et al., 2009; Lara-Chica et al., 2022). In cattle (Bos taurus) and yak (Bos mutus), the level of CDC25A in the testis can influence the fertility traits (Li-Yan et al., 2009). In human, the CDC25A can influences the mammary tumors development (Sur and Agrawal, 2016).

Saburai or Boerawa is one of local goat breeds in Indonesia that developed from the grading-up of Boer bucks (75%) and Ettawa grade does (25%). Saburai has been decided as the local goat breeds since 2015 through the decision of Indonesian Ministry of Agriculture No: 359/Kpts/PK.040/6/2015 (Kementan RI, 2015). Saburai goats were kept for meat production purpose with the adult weight of 38.00±3.78 kg in males and 32.10±11.43 kg in females (Kusuma et al., 2020; Dakhlan et al., 2021). Previously, many studies have been investigated the genetic markers in Saburai goats. As a results, two candidate genes of Leptin (LEP) and P21-Activated Kinase (PAK1) in thats goats had low genetic diversity and monomorphic, respectively (Nur et al., 2019; Damayanti et al., 2023). Therefore, the Growth hormone (GH) and Myostatin (MSTN) of Saburai goats had high genetic diversity and can be used as genetic marker for growth traits (Sulastri et al., 2019; Dakhlan et al., 2023). Previously, an indel 20 bp mutation at intron 9 (g.13971_13992indel.20) of caprine CDC25A gene had the significance association with growth traits and litter size of goats (Cui et al., 2019; Yang et al., 2021). Presently, no study to investigate the genetic diversity of CDC25A gene in Saburai goats. Hence, the present study was aimed to detect the indel 20 bp mutation in caprine CDC25A gene of Saburai goats and its association with growth traits. The results of this study are important to obtain the genetic markers for productivity traits of Saburai goats in the future.

2. Materials and Methods

2.1. Approval ethics

The animal ethics protocol in this study was approved by the Faculty of Agriculture, University of Lampung (Certificate No: 6410/UN26.14/2023).

2.2. Research site

The Saburai does in this study was collected from the Villager Breeding Center (VBC) at Tanggamus Regency, Lampung Province of Indonesia. This area is placed at about 246 m asl with the astronomical location at latitude 5° 05’-5° 56’ S and longitude 104° 18’-105° 12’ E. In general, this area had 27.3-29.6 °C of air temperature; 72.1-81.8% of relative humidity and 2,066 mm of rainfall per year.

2.3. Animals and DNA extraction

Twenty-four (24) blood samples (±5 mL/sample) were taken from the jugular vein of Saburai does using venoject needles and vacutainer tube containing EDTA. Therefore, the blood samples were stored in freezer at -20 °C until further analysis. The DNA extraction analysis was performed using a Genomic DNA Extraction Kit (Geneaid, Taiwan) following the manufacturer’s instructions.

2.4. Data records and management of animal

The data records of birth weight, weaning weight (4 months of age), yearling weight (12 months of age) and preweaned/postweaned daily weight gain were collected from the herd books. In general, the feed ration in animal under study consisted of gamal (Gliricidia sepium), kaliandra (Calliandra calothyrsus), and Elephant grass (Pennisetum purpureum). The feeding schedule is three times a day: morning, noon, and afternoon. The does were kept in a pen with ad libitum water. The natural mating and artificial mating were managed in the Saburai does using similar breed of bucks.

2.5. PCR, genotyping and sequencing

The amplification of caprine CDC25A gene (274/294 bp) was performed in total volume of 10 µL containing of 3 µL of DNA template; 5 µL of PCR mastermix; 0.2 µL of each primer (10 pmol) and 1.6 µL of free-nuclease water. The primer pairs in the present study was designed with Primer3Plus program (www.primer3plus.com) as follows: Forward: 5′- TGC ATT TTT CTT GTG TCC TGA -3′ and Reverse: 5′- TCA GAT TTG TGG GGT TAC CAG -3′. The target sequence and primer pairs position were illustrated in Figure 1. Therefore, a PCR analysis was performed in 1 cycle of pre-denaturation at 95 °C for 2 minutes and followed by 40 cycles of denaturation at 95 °C for 1 minute and 30 seconds; annealing at 58.5 °C for 1 minute; initial extension at 72 °C for 1 minute and final extension at 72 °C for 5 minutes. Visualization of the PCR product was performed through electrophoresis analysis on 100 V for 35 minutes with 2% of agarose gel containing 2 µL of DNA staining and captured by Gell Documentation System (Uvitec, UK). Therefore, Genotyping in the indel 20 bp locus was performed based on the patterns of DNA fragment i.e. 1 DNA fragment along 274 bp and 294 bp as DD and II genotypes, respectively. While, the ID genotype signed by 2 DNA fragments along 274 bp and 294 bp. To clarify the indel 20 bp case in Saburai does, two samples of II and DD genotypes (30 µL/sample) were used for the sequencing analysis through 1^st BASE Laboratory Services (Malaysia).

Figure 1
Primer position (blue and green) and the indel 20 bp mutation (red) in the target sequence of caprine CDC25A gene (GenBank: NC_030829.1) along 294 bp (intron 9).

2.6. Data correction

The data records of growth traits were corrected to reduce the data variation referring to Sulastri et al. (2019) as follows (Equations 1 to 5):

$$B{W}_c=BW\left(C{F}_{TB}\right)$$ (1)

$$W{W}_c=BW+\left\{\left[\left(WW-BW\right)/T_w\right]\times 90\right\}\left(C{F}_{DA}\right)\left(C{F}_{TB}\right)$$ (2)

$$Y{W}_c=W{W}_c+\left\{\left[\left(YW-WW\right)/T_y\right]\times 245\right\}$$ (3)

$$ADG1=\left(W{W}_c-B{W}_c\right)/90$$ (4)

$$ADG2=\left(Y{W}_c-W{W}_c\right)/245$$ (5)

where, WW_c is the corrected weaning weight; YW_c is the corrected yearling weight; BW_c is the corrected birth weight; BW is the actual birth weight; WW is the actual weaning weight; YW is the actual yearling weight; ADG1 is the preweaned daily gain; ADG2 is the postweaned daily gain; T_w is the period from birth to weaned; and T_y is the period from weaning to yearling age.

2.7. Data analysis

The genetic diversity parameters of genotype frequency, allele frequency, observed heterozygosity (H_o), expected heterozygosity (H_e), polymorphic informative content (PIC), number of effective allele (n_e) and Chi-square (χ²) values were calculated referring to Nei and Kumar (2000). In addition, the association study for detecting the effect of CDC25A gene polymorphism to the growth traits of does, was analyzed using a general linear model (GLM) with mathematical Formula 6:

$$Y_{ij}=\mu +G_i+E_{ij}$$ (6)

where, Y_ij is the observed value; μ is the common means; G_i is the effect of i^th genotype and E_ij is the experimental error.

3. Results and Discussion

The amplification of CDC25A gene in Saburai goats reveals three genotype of DD, ID and II as shown in Figure 2. In Saanbei White Cashmere (SWC) goats, the DD genotype of CDC25A gene was not observed (Cui et al., 2019; Yang et al., 2021). An indel 20 bp sequence of TCA CTG GAA GTT GTA CAT TT was detected in the CDC25A gene of Saburai goat (Figure 3). The insertion and deletion sequences of Saburai CDC25A gene have been deposited in the GenBank database with the accession number of LC860863 and LC860864, respectively. According to the target sequence (Figure 1), the indel 20 bp mutation spread from 13972^th to 13991^th nucleotide. The D allele was detected as the superior allele (0.65) as shown in Table 1. The n_e value was 1.84 and indicated that the indel 20 bp locus in CDC25A gene of Saburai goats had two common allele (D and I). In addition, the PIC value in the indel 20 bp locus of Saburai CDC25A gene was 0.35 and represented of high genetic diversity in the indel 20 bp locus of caprine CDC25A gene. This value explained that polymorphism of indel 20 bp in caprine CDC25A gene had the potency for molecular selection in Saburai goats based on this preliminary study. According to Nei and Kumar (2000), the PIC can be classified in low (<0.20), moderate (0.20 - 0.30) and high (>0.30) categories. Hence, polymorphism of indel 20 bp in caprine CDC25A had the potency as the genetic markers for economic traits of Saburai goats. The Chi-square (χ²) value in the investigated locus was under the genetic equilibrium and indicated that no previous selection affecting the allele frequency in this locus. In this study, the polymorphism in the CDC25A gene was not significance associated with the growth traits of Saburai does (Table 2). However, the average of birth weight, weaning weight, yearling weight and postweaned daily weight gain in II does were the highest than DD and II does. While, the does with DD had the lowest of growth traits rather than other genotype.

Figure 2
The amplification of CDC25A gene (294 bp) in Saburai goats on 2% agarose gel reveals three genotypes of DD (274 bp), ID (274 bp and 294 bp) and II (294 bp). M: DNA ladder 100 bp.

Figure 3
Detection an indel mutation 20 bp at intron 9 region of Saburai CDC25A gene.

Table 1
Genetic diversity in the indel 20 bp locus of CDC25A2 gene in Saburai goat.

Genotype frequency (N)			Allele frequency		Ho	He	PIC	ne	χ2
DD	ID	II	D	I
0.46 (11)	0.37 (9)	0.17 (4)	0.65	0.35	0.37	0.46	0.35	1.84	0.78*

• N: number of observation; H_o: observed heterozygosity; H_e: expected heterozygosity; PIC: polymorphic informative content; n_e: number of effective allele; χ²: Chi-square value;
• ^*
  under the genetic equilibrium.

Table 2
Association of indel 20 bp locus at intron 9 of CDC25A gene with growth traits in Saburai does.

Growth traits	Genotype
	DD (N=11)	ID (N=9)	II (N=4)
Birth weight (kg)	2.85±0.75	3.19±0.95	3.23±0.39
Weaning weight (kg)	15.41±2.99	16.76±3.82	16.94±1.60
Yearling weight (kg)	33.23±8.97	37.31±11.43	37.79±4.77
Preweaned daily weight gain (kg/day)	0.10±0.02	0.11±0.02	0.11±0.01
Postweaned daily weight gain (kg/day)	0.07±0.02	0.08±0.03	0.09±0.01

• N: number of animal.

Unfortunately, study to investigate the effect of CDC25A gene polymorphism to the economic traits of goats is limited. In SWC goats, an indel 20 bp polymorphism in CDC25A gene had the significance association with height at hip and cannon circumference. In this case, the II goats had the higher of body measurements than ID goats (Cui et al., 2019). Despite this, SWC goats with II genotype had the higher of first born litter size than ID genotype (Yang et al., 2021). Hence, the II genotype is seen as the best genotype and similar to the present study. Many studies reported that the indel mutation site at the intron region were used as the genetic marker for economic traits of goats such as: indel 7 bp mutation (intron 3) in A-kinase anchoring protein (AKAP12) gene (Kang et al., 2021), indel 11 bp mutation (intron 22) in DNA methyltransferase 3 β (DNMT3B) gene (Hui et al., 2020), indel 5 bp (intron 2) and indel 10 bp (intron 5) mutations in Janus kinase 2 (JAK2) gene (Wu et al., 2024b), indel 22 bp mutation (intron 2) in Fibroblast growth factor 7 (FGF7) gene (Wu et al., 2024a), and indel 4 bp (intron 3 and intron 7) and 6 bp (intron 23) in Cilia and flagella associated protein 43 (CFAP43) gene (Mi et al., 2022).

Moreover, previous studies reported many indel mutation sites in the candidate genes of SWC goats. Zhao et al. (2024) was found 5 indel mutation sites in intron 2 (3 sites) and intron 3 (2 sites) regions of Yes-associated protein (YAP) in SWC goats. Despite this, 3 indel mutation sites (1 site in intron 2 and 2 sites in intron 3) were detected in Transcriptional co-activator with PDZ-binding motif (TAZ) gene of SCW goats. Bi et al. (2022) found 2 indel mutation sites (17 bp and 21 bp) in the intronic region of Sorting nexin 29 (SNX29) in SWC goats. Despite of intron region, an indel 22 bp mutation site WAS FOUND in the promoter region of Paired-like homeodomain 2 (PITX2) gene of SCW goats (Yan et al., 2018). Subsequently, 2 indel mutation sites at intron 2 (15 bp) and 3’UTR (5 bp) regions were reported in Insulin-like growth factor 2 mRNA binding protein 1 (IGF2BP1) of SWC goats (Wang et al., 2020). Liu et al. (2019) found an indel 21 bp in the Scribble cell polarity complex component (LLGL1) gene of SWC goats and also used for the genetic marker.

The existence of introns in the genome is important in various cellular processes such as splicing, mRNA transport, nonsense-mediated decay (NMD), expression regulation and transcription initiation (Chorev and Carmel, 2012; Jo and Choi, 2015). Besides, introns may give some advantages as a mutational buffer in eukaryotic genomes protecting coding sequences from being affected by randomly occurring deleterious mutations. (Jo and Choi, 2015). Interestingly, the genome-wide association study (GWAS) revealed that most of the single nucleotide polymorphisms (SNPs) have been mapped to intron regions rather than exonic or nonsysnonymous sites (Welter et al., 2014).

Related to the growth traits, the CDC25A gene encodes many proteins such as dihydrofolate reductase (DHFR), thymidine kinase (TK), and ribonucleotide reductase (RR), which commonly share similar E2F binding sites in their promoters (DeGregori et al., 1995). The binding of E2F transcription factors are key regulator of cell proliferation (Attwooll et al., 2004) and the cell cycle progression (Blais and Dynlacht, 2007).

Previously, Dakhlan et al. (2023) reported an indel mutation of g.641_642indel.T in the intron 2 of Saburai MSTN gene and had the potency as the genetic marker for growth traits. In this study, the DD genotype was observed with the highest frequency (0.46) and followed by ID (0.37) and II (0.17) genotypes. In contrast, DD genotype was absence in SWC goats. Hence, the indel 20 bp locus in CDC25A gene of Saburai goats is not a conservative site with high genetic diversity. The different of genotype characteristics between Saburai and SWC goats can be caused by genetics composition, environment and selection factors. The further study involving large sample is important to confirm the effect of CDC25A gene polymorphism to the growth traits of Saburai goats.

4. Conclusion

The indel 20 bp mutation of CDC25A gene (intron 9) was observed in the Saburai does under study. The indel 20 bp locus in CDC25A gene of Saburai does had high genetic diversity with presence of DD, ID and II genotypes. Nonetheless, no significance association between CDC25A gene polymorphism and the growth traits of Saburai does in this preliminary study. In the future, in-dept study to confirm the effectiveness of indel 20 bp locus in Saburai CDC25A gene with large samples is important to develop a molecular selection in this goat.

Acknowledgements

Authors thank to the Saburai goat farmers at Tanggamus District, Lampung for the permission to collect bloods sample of goat.

Data Availability Statement

The research data is available upon prior request via email to the corresponding author.

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Edited by

• Editor:
  Takako Matsumura Tundisi

Publication Dates

• Publication in this collection
  10 July 2026
• Date of issue
  2026

History

• Received
  15 Jan 2026
• Accepted
  25 Mar 2026