两广小花猪FOXL2基因多态性及其与几个重要经济性状的关联分析

doi:10.11843/j.issn.0366-6964.2023.03.010

畜牧兽医学报 ›› 2023, Vol. 54 ›› Issue (3): 956-965.doi: 10.11843/j.issn.0366-6964.2023.03.010

两广小花猪FOXL2基因多态性及其与几个重要经济性状的关联分析

廖伟莉¹, 张笑科¹, 曾检华², 阳林芳², 李硕¹, 胡梦婷¹, 郭懿萱¹, 陈赞谋¹, 张豪¹, 李加琪¹, 袁晓龙^1*

1. 华南农业大学动物科学学院, 广东省农业动物基因组学与分子育种重点实验室, 国家生猪种业工程技术研究中心, 广州 510642;
2. 广东壹号地方猪研究院有限公司, 湛江 524000

收稿日期:2022-08-17 出版日期:2023-03-23 发布日期:2023-03-21
通讯作者: 袁晓龙,主要从事动物遗传育种研究,E-mail:yxl@scau.edu.cn
作者简介:廖伟莉(1997-)，女，广东梅州人，硕士生，主要从事动物遗传育种研究，E-mail：laoveli1028@163.com
基金资助:
广东省重点领域研发计划(2022B0202090002)；财政部和农业农村部：国家现代农业产业技术体系资助(CARS-35)；国家自然科学基金(32072694)；广东省自然科学基金(2021A1515012396)；广州市科技计划项目(202002030071)

Associations between FOXL2 Polymorphism and Several Important Economic Traits in Liangguang Spotted Pigs

LIAO Weili¹, ZHANG Xiaoke¹, ZENG Jianhua², YANG Linfang², LI Shuo¹, HU Mengting¹, GUO Yixuan¹, CHEN Zanmou¹, ZHANG Hao¹, LI Jiaqi¹, YUAN Xiaolong^1*

1. National Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-animal Genomics and Molecular Breeding, College of Animal Sciences, South China Agricultural University, Guangzhou 510642, China;
2. Guangdong Yihao Indigenous Pig Research Institute Co. Ltd., Zhanjiang 524000, China

Received:2022-08-17 Online:2023-03-23 Published:2023-03-21

摘要/Abstract

摘要： 旨在筛选FOXL2(forkhead box protein L2)基因与猪排卵状态和屠宰性状相关的SNPs位点，为今后两广小花猪分子育种和遗传改良提供理论和参考依据。本研究以107头(365±25)日龄两广小花猪为研究对象，使用靶向测序基因型检测(genotyping by target sequencing，GBTS)技术定位FOXL2基因的SNPs位点，对排卵状态、乳头数和屠宰性状进行关联分析和单倍型分析。两广小花猪FOXL2基因共检测到24个突变位点。剔除InDel突变和突变频率小于1%的SNP位点后，对得到的12个SNPs进行关联分析，其中2个位于编码区、10个位于非编码区。单SNP位点关联分析表明，g.79706726 T>C、g.79706898 C>T、g.79707794 T>C、g.79709005 T>C这4个位点对排卵状态均有显著性影响(P<0.05)，对总乳头数性状无显著性影响(P>0.05)。g.79707040 A>G、g.79708079 T>C、g.79708152 G>T、g.79706726 T>C、g.79706898 C>T、g.79707794 T>C这6个SNPs位点对骨重、瘦肉率、腿臀重、左胴体重性状均有显著性影响(P<0.05)，其中3个SNPs位点g.79707040 A>G、g.79708079 T>C、g.79708152 G>T对板油重性状有显著性影响(P<0.05)。SNP位点单倍型组合关联分析发现，g.79706726 T>C、g.79706898 C>T、g.79707794 T>C这3个位点处于强连锁区域内(r²>0.9)。H1H2单倍型组合(g.79706726 T>C和g.79706898 C>T)对排卵状态、骨重、瘦肉率、腿臀重、左胴体重性状均有显著性影响(P<0.05)，其中CCTT单倍型个体的骨重、腿臀重和左胴体重性状显著高于TTCC单倍型个体(P<0.05),CCTT单倍型个体的瘦肉率性状显著低于TTCC单倍型个体(P<0.05)。FOXL2基因中有与排卵状态显著相关的g.79706726 T>C、g.79706898 C>T、g.79707794 T>C、g.79709005 T>C等SNPs位点。另外，本研究发现了FOXL2转录因子与猪屠宰性状相关的SNPs位点，表明FOXL2转录因子除了维持卵巢表型和功能以外，还影响猪的重要经济性状。本研究为FOXL2基因在两广小花猪的选种选育中提供重要参考，为分子标记辅助选择提供理论依据。

关键词: 卵巢, 屠宰性状, FOXL2, SNPs, 单倍型

Abstract: The purpose of this study was to explore the SNPs of FOXL2 gene and their effects on ovulation status and slaughtering traits, in order to provide theoretical basis for molecular breeding and genetic improvement of Liangguang Spotted pigs in the future. A total of 107 Liangguang Spotted pigs at the age of (365±25) days were taken as the research objects. The SNPs of FOXL2 were detected using genotyping by target sequencing (GBTS) technology, and association analysis and haplotype analysis were performed on ovulation status, teat numbers and slaughter traits. A total of 24 mutation sites were detected in the FOXL2 gene of Liangguang Spotted pigs. After eliminating SNPs with InDel mutation and the mutation frequency less than 1%, 12 SNPs were analyzed. Among them, 2 SNPs were located in the coding region and 10 SNPs were located in the non-coding region. The association analysis showed that the g.79706726 T>C, g.79706898 C>T, g.79707794 T>C, and g.79709005 T>C showed significant effects on ovulation status (P＜0.05), but had no significant effects on teat numbers trait (P >0.05). The 6 SNPs (g.79707040 A>G, g.79708079 T>C, g.79708152 G>T, g.79706726 T>C, g.79706898 C>T, and g.79707794 T>C) had significant effects on bone weight, lean meat rate, ham weight, and left carcass weight (P＜0.05), and 3 SNPs (g.79707040 A>G, g.79708079 T>C, g.79708152 G>T) displayed significant effects on leaf fat weight (P<0.05). The associa-tion analysis of haplotype combination found that the 3 SNPs g.79706726 T>C, g.79706898 C>T, and g.79707794 T>C were strongly linked (r²>0.9). The H1H2 haplotype combination (g.79706726 T>C and g.79706898 C>T) had significant effects on ovulation status, bone weight, lean meat rate, ham weight, and left carcass weight (P<0.05). The bone weight, ham weight, and left carcass traits of individuals with CCTT haplotype were significantly higher than those with TTCC haplotype (P<0.05), and the lean meat rate trait of individuals with CCTT haplotype was significantly lower than those wtih TTCC haplotype (P<0.05). Four SNPs of FOXL2 gene were significantly associated with ovulation status, which were g.79706726 T>C, g.79706898 C>T, g.79707794 T>C, and g.79709005 T>C. In addition, the SNPs of FOXL2 associated with pig slaughter traits were found in this study, indicating that FOXL2 was not only associated with ovarian phenotype and function, but also relevant for pig growth and development. This study provided an important reference for the selection and breeding of FOXL2 gene in Liangguang Spotted pigs, and also provided a theoretical basis for molecular marker-assisted breeding.

Key words: ovary, slaughtering traits, FOXL2, SNPs, haplotype

中图分类号:

S828.2

廖伟莉, 张笑科, 曾检华, 阳林芳, 李硕, 胡梦婷, 郭懿萱, 陈赞谋, 张豪, 李加琪, 袁晓龙. 两广小花猪FOXL2基因多态性及其与几个重要经济性状的关联分析[J]. 畜牧兽医学报, 2023, 54(3): 956-965.

LIAO Weili, ZHANG Xiaoke, ZENG Jianhua, YANG Linfang, LI Shuo, HU Mengting, GUO Yixuan, CHEN Zanmou, ZHANG Hao, LI Jiaqi, YUAN Xiaolong. Associations between FOXL2 Polymorphism and Several Important Economic Traits in Liangguang Spotted Pigs[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(3): 956-965.

参考文献 40

[1]	GARCIA-ORTIZ J E,PELOSI E,OMARI S,et al.Foxl2 functions in sex determination and histogenesis throughout mouse ovary development[J].BMC Dev Biol,2009,9:36.
[2]	SINCLAIR A,SMITH C.Females battle to suppress their inner male[J].Cell,2009,139(6):1051-1053.
[3]	徐超,李凤,郝海生,等.性别相关基因在牛早期性别发育中的表达规律研究[J].畜牧兽医学报,2017,48(10):1892-1901.XU C,LI F,HAO H S,et al.Sex-related genes expression during development of the early bovine fetuses[J].Acta Veterinaria et Zootechnica Sinica,2017,48(10):1892-1901.(in Chinese)
[4]	SCHMIDT D,OVITT C E,ANLAG K,et al.The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance[J].Development,2004,131(4):933-942.
[5]	MORK L,MAATOUK D M,MCMAHON J A,et al.Temporal differences in granulosa cell specification in the ovary reflect distinct follicle fates in mice[J].Biol Reprod,2012,86(2):37.
[6]	BERNARD D J,TRAN S.Mechanisms of activin-stimulated FSH synthesis:the story of a pig and a FOX[J].Biol Reprod,2013, 88(3):78.
[7]	BILEZIKJIAN L M,JUSTICE N J,BLACKLER A N,et al.Cell-type specific modulation of pituitary cells by activin,inhibin and follistatin[J].Mol Cell Endocrinol,2012,359(1-2):43-52.
[8]	DIAS J A,ULLOA-AGUIRRE A,BOUSFIELD G R,et al.Editorial for the MCE special issue on "Novel endocrine mechanisms in the regulation of reproduction" [J].Mol Cell Endocrinol,2014,382(1):385-386.
[9]	ODLE A K,CHILDS G V.SMAD-FOXL2 regulation of FSHB:a game of human and mouse[J].Endocrinology, 2020,161(7):bqaa077.
[10]	UHLENHAUT N H,TREIER M.Forkhead transcription factors in ovarian function[J].Reproduction,2011,142(4):489-495.
[11]	RAY P S,WANG J H,QU Y,et al.FOXC1 is a potential prognostic biomarker with functional significance in basal-like breast cancer[J].Cancer Res,2010,70(10):3870-3876.
[12]	KANG L J,YU Z H,CAI J,et al.Reciprocal transrepression between FOXF2 and FOXQ1 controls basal-like breast cancer aggressiveness[J].FASEB J,2019,33(5):6564-6573.
[13]	WEGMAN P,EREMO A G,LINDLÖF A,et al.Expression of the forkhead transcription factor FOXL2 correlates with good prognosis in breast cancer patients treated with tamoxifen[J].Int J Oncol,2011,38(4):1145-1151.
[14]	刘昱翔.FOXA2的互作蛋白FOXP2调控乳腺癌上皮间质转化的机制研究[D].长沙:湖南大学,2021.LIU Y X.The study of FOXA2-interacting transcription factor FOXP2 in regulating the epithelial-mesenchymal transition of breast cancer cells[D].Changsha:Hunan University,2021.(in Chinese)
[15]	BERNARDO G M,BEBEK G,GINTHER C L,et al.FOXA1 represses the molecular phenotype of basal breast cancer cells[J].Oncogene,2013,32(5):554-563.
[16]	ZHONG J T,WANG H J,YU J,et al.Overexpression of Forkhead Box L1(FOXL1) inhibits the proliferation and invasion of breast cancer cells[J].Oncol Res,2017,25(6):959-965.
[17]	朱猛进,钱云,丁家桐,等.母猪FSHβ基因多态与乳头数的关系研究[J].畜牧与兽医,2000,32(3):12-14.ZHU M J,QIAN Y,DING J T,et al.A study on the relationship between polymorphisms of sows'FSHβ gene and their teat numbers[J].Animal Husbandry&Veterinary Medicine,2000,32(3):12-14.(in Chinese)
[18]	ROPKA-MOLIK K,BERETA A,ŻUKOWSKI K,et al.Screening for candidate genes related with histological microstructure,meat quality and carcass characteristic in pig based on RNA-seq data[J].Asian-Australas J Anim Sci,2018, 31(10):1565-1574.
[19]	潘泽滚,李志雄.藏鸡FoxO1基因多态性及与屠宰和生长性状的关联分析[J].中国家禽,2022,44(4):13-21.PAN Z G,LI Z X.Polymorphisms of FoxO1 gene related to growth and slaughter traits in Tibetan chicken[J].China Poultry,2022, 44(4):13-21.(in Chinese)
[20]	王玲.普通牛FoxO1、FoxO3、FoxO4基因的克隆、表达及其对肉质性状的遗传效应分析[D].雅安:四川农业大学,2010.WANG L.Cloning,expression and genetic effects of bovine FoxO1,FoxO3 and FoxO4 genes on meat quality traits[D].Yaan:Sichuan Agricultural University,2010.(in Chinese)
[21]	曾检华,李闯,韦明飞,等.两广小花猪(壹号黑猪)新品系选育进展[J].养猪,2019(4):65-68.ZENG J H,LI C,WEI M F,et al.Porgress of breeding on Liang Guang Small-spotted Pig (Yihao Black Pig)[J].Swine Production, 2019(4):65-68.(in Chinese)
[22]	黄雅琼,江永强,梁文全,等.陆川猪的生物学特征及其优良性能的研究概况[J].家畜生态学报,2013,34(5):82-84.HUANG Y Q,JIANG Y Q,LIANG W Q,et al.A review of biological characteristics and performance in Luchuan pig[J].Acta Ecologiae Animalis Domastici,2013,34(5):82-84.(in Chinese)
[23]	薛尚军,杨晓奋,刘宏,等.中国地方猪种的肉质特性[J].国外畜牧学-猪与禽,2011,31(2):92-94.XUE S J,YANG X F,LIU H,et al.Meat quality characteristics of local pig breeds in China[J].Animal Science Abroad (Pigs and Poultry),2011,31(2):92-94.(in Chinese)
[24]	任红艳,胡景杰,杜生明.中国地方猪种成肌与肌内沉脂的遗传机制解析--国家自然科学基金重大项目介绍[J].畜牧兽医学报,2018,49(5):1096-1098.REN H Y,HU J J,DU S M.Genetic mechanisms of myogenesis and intramuscular adipogenesis in Chinese indigenous pigs-introduction to major program of The National Natural Science Foundation of China[J].Acta Veterinaria et Zootechnica Sinica,2018, 49(5):1096-1098.(in Chinese)
[25]	WANG K,LI M Y,HAKONARSON H.ANNOVAR:functional annotation of genetic variants from high-throughput sequencing data[J].Nucleic Acids Res,2010,38(16):e164.
[26]	中华人民共和国农业部.NY/T 825-2004瘦肉型猪胴体性状测定技术规范[S].北京:中国农业出版社,2004.The Ministry of Agriculture of the People's Republic of China.NY/T 825-2004 Technical regulation for testing of carcass traits in lean-type pig[S].Beijing:China Agriculture Press,2004.(in Chinese)
[27]	BARRETT J C,FRY B,MALLER J,et al.Haploview:analysis and visualization of LD and haplotype maps[J].Bioinformatics, 2005,21(2):263-265.
[28]	LIU X L,MENG Y H,WANG J L,et al.FOXL2 suppresses proliferation,invasion and promotes apoptosis of cervical cancer cells[J].Int J Clin Exp Pathol,2014,7(4):1534-1543.
[29]	BELLI M,SECCHI C,STUPACK D,et al.FOXO1 negates the cooperative action of FOXL2C134 W and SMAD3 in CYP19 expression in HGrC1 cells by sequestering SMAD3[J].J Endocr Soc,2019,3(11):2064-2081.
[30]	黄梅梅,尹如铁.FOXL2基因在卵巢颗粒细胞瘤中的研究现状[J].中华妇幼临床医学杂志(电子版),2019,15(3):349-352.HUANG M M,YIN R T.Current research status of FOXL2 gene in granulocytoma of ovary[J].Chinese Journal of Obstetrics&Gynecology and Pediatrics (Electronic Edition),2019,15(3):349-352.(in Chinese)
[31]	张昌政,李德森,黄敏,等.基于全基因组填充重测序关联分析鉴别影响苏山猪初生体尺与乳头数性状的遗传位点[J].畜牧兽医学报,2023,54(1):88-102.ZHANG C Z,LI D S,HUANG M,et al.An imputed whole-genome sequence-based GWAS approach pinpoints genetic loci for body conformation at birth and teat number traits in Sushan pig population[J].Acta Veterinaria et Zootechnica Sinica, 2023,54(1):88-102.(in Chinese)
[32]	KNOX R V.Physiology and endocrinology symposium:factors influencing follicle development in gilts and sows and management strategies used to regulate growth for control of estrus and ovulation[J].J Anim Sci,2019,97(4):1433-1445.
[33]	LAMBA P,WANG Y,TRAN S,et al.Activin a regulates porcine follicle-stimulating hormone β-subunit transcription via cooperative actions of SMADs and FOXL2[J].Endocrinology,2010,151(11):5456-5467.
[34]	熊冬梅,李蓉.抑制素、激活素、卵泡抑素与卵泡发育[J].华西医学,2006,21(1):188-189.XIONG D M,LI R.Inhibin,activin,follistatin and follicle development[J].West China Medical Journal,2006,21(1):188-189.(in Chinese)
[35]	SEACHRIST D D,KERI R A.The activin social network:activin,inhibin,and follistatin in breast development and cancer[J]. Endocrinology, 2019,160(5):1097-1110.
[36]	RECCHIA K,JORGE A S,DE FIGUEIREDO PESSÔA L V,et al.Actions and roles of FSH ingerminative cells[J].Int J Mol Sci,2021,22(18):10110.
[37]	中国地方猪品种资源介绍(一)[J].中国猪业,2006(2):20-22.Introduction of Chinese local pig breed resources (1)[J].China Swine Industry,2006(2):20-22.(in Chinese)
[38]	张家富.陆川猪若干种质特性基础研究[D].南宁:广西大学,2012.ZHANG J F.Basic research on several breeding characteristics in Luchuan pig[D].Nanning:Guangxi University,2012.(in Chinese)
[39]	PIERINI S,TANYI J L,SIMPKINS F,et al.Ovarian granulosa cell tumor characterization identifies FOXL2 as an immunotherapeutic target[J].JCI Insight,2020,5(16):e136773.
[40]	ACARÇEVIK U,KAYAÇAVUŞOǦLU B,SAǦLIK B N,et al.Synthesis,docking studies and biological activity of new benzimidazole-triazolothiadiazine derivatives as aromatase inhibitor[J].Molecules,2020,25(7):1642.

两广小花猪FOXL2基因多态性及其与几个重要经济性状的关联分析

Associations between FOXL2 Polymorphism and Several Important Economic Traits in Liangguang Spotted Pigs

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