Differential expression and genetic polymorphism of DMRT1 and FOXL2 genes in the gonads of Kadaknath chicken


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Authors

  • SHIVANI BACHAMOLLA College of Veterinary Science, PVNR Telangana Veterinary University, Hyderabad, Telangana image/svg+xml
  • JAYAKUMAR SIVALINGAM ICAR– Directorate of Poultry Research, Hyderabad, Telangana image/svg+xml
  • VELPULA CHINNIPREETAM College of Veterinary Science, PVNR Telangana Veterinary University, Hyderabad, Telangana image/svg+xml
  • DAIDA KRISHNA College of Veterinary Science, PVNR Telangana Veterinary University, Hyderabad, Telangana image/svg+xml
  • SHANMUGAM MURUGESAN ICAR–Directorate of Poultry Research, Hyderabad, Telangana image/svg+xml
  • B RAJITH REDDY ICAR–Directorate of Poultry Research, Hyderabad, Telangana image/svg+xml
  • TARUN KUMAR BHATTACHARYA NRC on Equines, Hisar, Haryana
  • RAJKUMAR ULLENGALA ICAR - Directorate of Poultary Research, Hyderabad, Telangana 500 030 India image/svg+xml

https://doi.org/10.56093/ijans.v94i7.149461

Keywords:

Chicken, DMRT1, FOXL2, Genetic polymorphism, Ovary, Relative gene expression

Abstract

In chicken, the left ovary is functional and the right ovary becomes rudimentary in the later stage of the embryonic development. The expression and genetic polymorphism of the DMRT1 and FOXL2 genes are assessed in order to understand the distinct developing process of gonads in male and female embryonic gonads. In the current study, 19th day Kadaknath chicken gonadal tissue samples were collected from the embryos and RT-PCR analysis and DNA sequencing was done. According to the expression studies, the left ovaries relative expression of FOXL2 was 2.14 and 12.65 factor greater than that of the right ovaries and testes, while the right testis relative expression of DMRT1 was 3.78 and 3.83 fold higher than that of the left and right ovaries. DNA sequence analysis in the left ovary identified a nonsynonymous alteration (c.289C>G) involving histidine to aspartic acid at the 289th position in the FOXL2 coding region. The 51st position of exon 6 of DMRT1 has a G→A transition SNP that is not part of the coding sequence (CDS). Males showed higher levels of the DMRT1 gene than females, while females expressed higher levels of FOXL2. It was found that the DMRT1 and FOXL2 genes are polymorphic. The genetic variability in the gonads and the differences in DMRT1 and FOXL2 gene expression allow learning more about the critical mechanisms underlying chicken gonadal development.

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References

Abu-Rekaiba R I A, Razuki W M and Al-Anbari E H. 2021. Polymorphic explore of Esr1, Esr2 and Foxl2 genes and interaction effect of Esri and Foxl2 with productive traits of Brown Local Iraqi chickens. In IOP Conference Series: Earth and Environmental Science 910(1): 012004.

Addess K J, Basilion J P, Klausner R D, Rouault T A and Pardi A. 1997. Structure and dynamics of the iron responsive element RNA: Implications for binding of the RNA by iron regulatory binding proteins. Journal of Molecular Biology 274(1): 72–83.

Allain F H T, Gubser C C, Howe P W, Nagai K, Neuhaus D and Varani G. 1996. Specificity of ribonucleoprotein interaction determined by RNA folding during complex formation. Nature 380(6575): 646–50.

Ayers K L, Davidson N M, Demiyah D , Roeszler K N, Grützner F, Sinclair A H and Smith C A. 2013. RNA sequencing reveals sexually dimorphic gene expression before gonadal differentiation in chicken and allows comprehensive annotation of the W-chromosome. Genome Biology 14(3): 1–17.

Bradley K M, Breyer J P, Melville D B, Broman K W, Knapik E W and Smith J R. 2011. An SNP-based linkage map for zebra fish reveals sex determination loci. G3: Genes| Genomes| Genetics 1(1): 3–9.

BratuśA,NeuenschwanderS,Piestrzyńska-KajtochA,Świtoński M, Klukowska-Roetzler J, and Słota E. 2011. Polymorphisms in DMRT1 coding and promoter regions are probably not causative for swine sex reversal (XX, SRY-negative) syndrome. Annals of Animal Science 11(1):17–26.

Burland T. G. 1999. DNASTAR’s Laser gene sequence analysis software. In Bioinformatics Methods and Protocols 132: 71– 91.

Carlon N and Stahl A. 1985. Origin of the somatic components in chick embryonic gonads. Archives d’anatomie Microscopiqueet de Morphologie Expérimentale 74(1): 52–59.

Chomczynski P and Sacchi N. 2006. The single-step method of RNA isolation by acid guanidinium thiocyanate–phenol– chloroform extraction: Twenty-something years on. Nature Protocols 1(2): 581–85.

Cocquet J, Pailhoux E, Jaubert F, Servel N, Xia X, Pannetier M and Veitia R A. 2002. Evolution and expression of FOXL2. Journal of Medical Genetics 39(12): 916–21.

Coleman T Pand Roesser J R. 1998. RNA secondary structure: An important cis-element in rat calcitonin/CGRP pre-messenger RNA splicing. Biochemistry 37(45): 15941–5950.

Crisponi L, Deiana M, Loi A, Chiappe F, Uda M, Amati P and Pilia G. 2001. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nature Genetics 27(2):159–66.

Cui Y, Wang W, Ma L, Jie J, Zhang Y, Wang H and Li H. 2018. New locus reveals the genetic architecture of sex reversal in the Chinese tongue sole (Cynoglossus semilaevis). Heredity 121(4): 319–26.

Denayer E, Parret A, Chmara M, Schubbert S, Vogels A, Devriendt K and Legius E. 2008. Mutation analysis in Costello syndrome: Functional and structural characterization of the HRAS p. Lys117Arg mutation. Human Mutation 29(2): 232–39.

Ellegren H. 2000. Evolution of the avian sex chromosomes and their role in sex determination. Trends in Ecology and Evolution 15(5): 188–92

Govoroun M S, Pannetier M, Pailhoux E, Cocquet J, Brillard J P, Couty I and Cotinot C. 2004. Isolation of chicken homolog of the FOXL2 gene and comparison of its expression patterns with those of aromatase during ovarian development. Developmental dynamics: An official publication of the American Association of Anatomists 231(4): 859–70.

Guo Y, Cheng H, Huang X, Gao S, Yu H and Zhou R. 2005. Gene structure, multiple alternative splicing, and expression in gonads of zebra fish DMRT1. Biochemical and Biophysical Research Communications 330(3): 950–57.

Hall T, Biosciences I and Carlsbad C J G B B. 2011. BioEdit: Important software for molecular biology. GERF Bulletin of Biosciences 2(1): 60–61.

Herpin A, Nakamura S, Wagner T U, Tanaka M and Schartl M. 2009. A highly conserved cis-regulatory motif directs differential gonadal syn expression of Dmrt1 transcripts during gonad development. Nucleic Acids Research 37(5): 1510–520.

Hodgkin J. 2002. The remarkable ubiquity of DM domain factors as regulators of sexual phenotype: Ancestry or aptitude. Genes and Development 16(18): 2322–326.

Hudson Q J, Smith C A and Sinclair A H. 2005. Aromatase inhibition reduces expression of FOXL2 in the embryonic chicken ovary. Developmental dynamics: An official publication of the American Association of Anatomists 233(3): 1052–055.

Ioannidis J, Taylor G, Zhao D, Liu L, Idoko-Akoh A, Gong D and Clinton M. 2021. Primary sex determination in birds depends on DMRT1 dosage, but gonadal sex does not determine adult secondary sex characteristics. Proceedings of the National Academy of Sciences 118(10): 1–10.

Kettlewell J R, Raymond C S and Zarkower D. 2000. Temperature dependent expression of turtle DMRT1 prior to sexual differentiation. Genesis 26(3): 174–78.

Koba N, Ohfuji T, Ha Y, Mizushima S, Tsukada A, Saito N and Shimada K. 2008. Profiles of mRNA expression of FOXL2, P450arom, DMRT1, AMH, P450c17, SF1, ERα and AR, in relation to gonadal sex differentiation in duck embryo. The Journal of Poultry Science 45(2):132–38.

Loffler K A, Zarkower D and Koopma P. 2003. Etiology of ovarian failure in blepharophimosis ptosis epicanthus inversus syndrome: FOXL2 is a conserved, early-acting gene in vertebrate ovarian development. Endocrinology 144(7): 3237–243.

LuoW, Gu L, Li J and Gong Y. 2020. Transcriptome sequencing revealed that knocking down FOXL2 affected cell proliferation, the cell cycle, and DNA replication in chicken pre-ovulatory follicle cells. PLoS One 15(7): 1–19.

Oréal E, Mazaud S, Picard J Y, Magre S and CarréEusèbe D. 2002. Different patterns of anti Müllerian hormone expression, as related to DMRT1, SF1, WT1, GATA4, Wnt4, and Lhx9 expression, in the chick differentiating gonads. Developmental dynamics: An official publication of the American Association of Anatomists 225(3): 221–32.

Pannetier M , Servel N , Cocquet J , Besnard N, Cotinot C and Pailhoux E. 2003. Expression studies of the PIS-regulated genes suggest different mechanisms of sex determination within mammals. Cytogenetic and Genome Research 101 (3-4): 199–205.

Pailhoux E, Vigier B, Chaffaux S, Servel N, Taourit S, Furet J. P and Vaiman D. 2001. A 11.7-kb deletion triggers intersexuality and polledness in goats. Nature Genetics 29(4): 453–58.

Picard M A L, Cosseau C, Mouahid G, Duval D , Grunau C, Toulza E and Boissier J. 2015. The roles of Dmrt (Double sex/Male-abnormal-3 Related Transcription factor) genes in sex determination and differentiation mechanisms: Ubiquity and diversity across the animal kingdom. Comptes Rendus Biologies 338(7): 451–62.

Qin N, Liu Q, Zhang Y Y, Fan X C, Xu X X, Lv Z C and Xu R F. 2015. Association of novel polymorphisms of forkhead box L2 and growth differentiation factor-9 genes with egg production traits in local Chinese Dagu hens. Poultry Science 94(1): 88–95.

Raghuveer K, Senthilkumaran B, Sudhakumari C C, Sridevi P, Rajakumar A,Singh R and Majumdar K C.2011. Dimorphic expression of various transcription factor and steroidogenic enzyme genes during gonadal ontogeny in the air-breathing catfish, Clarias gariepinus. Sexual Development 5(4): 213–23.

Schmidt D, Ovitt C E, Anlag K, Fehsenfeld S , Gredsted L, Treier A C and Treier M. 2004. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131(4): 933–42.

Shan Z, Nanda I, Wang Y, Schmid M, Vortkamp A and Haaf T. 2000. Sex-specific expression of an evolutionarily conserved male regulatory gene, DMRT1, in birds. Cytogenetic and Genome Research 89(3-4): 252–57.

Shen L X and Tinoco Jr I. 1995. The structure of an RNA pseudoknot that causes efficient frameshifting in mouse mammary tumour virus. Journal of Molecular Biology 247(5): 963–78.

Shi B, Wen H S, He F, Dong S L, Ma S, Chen C F and Zhou Y G. 2009. Association of reproductive performance with SNPs of FOXL2 gene by SSCP in Japanese flounder (Paralichthys olivaceus). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 153(1): 1–7.

Smith C A, Katz M and Sinclair A H. 2003. DMRT1 is upregulated in the gonads during female-to-male sex reversal in Z W chicken embryos. Biology of Reproduction 68(2): 560–70.

Smith C A, McClive P J, Western P S, Reed K J and Sinclair A H. 1999. Conservation of a sex-determining gene. Nature 402(6762): 601–02.

Uda M, Ottolenghi C, Crisponi L, Garcia J E, Deiana M, Kimber W and Pilia G. 2004. Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Human Molecular Genetics 13(11): 1171–181.

Von Bülow R, Schmidt B, Dierks T, Schwabauer N, Schilling K, Weber E and Von Figura K. 2002. Defective oligomerization of arylsulfatase a as a cause of its instability in lysosomes and metachromatic leukodystrophy. Journal of Biological Chemistry 277(11): 9455–461.

Yamamoto I, Tsukada A, Saito N and Shimada K. 2003. Profiles of mRNA expression of genes related to sex differentiation of the gonads in the chicken embryo. Poultry Science 82(9): 1462–467.

Yang Y, Gong P, Feng Y P, Li S J, Peng X L, Ran Z P, Qian Y G and Gong Y Z. 2013. Temporospatial expression of DMRT1 in chicken urogenital system (Gallus gallus) using whole mount in situ hybridization. Acta Biologica Hungarica 64(2): 161–68.

Zhang S O, Mathur S, Hattem, G, Tassy O and Pourquié O. 2010. Sex-dimorphic gene expression and ineffective dosage compensation of Z-linked genes in gastrulating chicken embryos. BMC Genomics 11(1): 1–13.

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2024-03-11

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2024-07-11

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BACHAMOLLA, S. ., SIVALINGAM, J. ., CHINNIPREETAM, V. ., KRISHNA, D. ., MURUGESAN, S. ., REDDY, B. R. ., BHATTACHARYA, T. K. ., & ULLENGALA, R. . (2024). Differential expression and genetic polymorphism of DMRT1 and FOXL2 genes in the gonads of Kadaknath chicken. The Indian Journal of Animal Sciences, 94(7), 620–625. https://doi.org/10.56093/ijans.v94i7.149461
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