Proteomic study of large and small testes in Ningdu Yellow chicken based on tandem mass tags(TMT) technology

doi:10.3969/j.issn.1004-1524.20240463

Acta Agriculturae Zhejiangensis ›› 2025, Vol. 37 ›› Issue (5): 1029-1044.DOI: 10.3969/j.issn.1004-1524.20240463

• Animal Science • Previous Articles Next Articles

Proteomic study of large and small testes in Ningdu Yellow chicken based on tandem mass tags(TMT) technology

MA Jing'e(), WU Siqi, WAN Shumin, XIONG Xinwei, XU Jiguo, XU Jing, RAO Yousheng, ZHOU Min()

Jiangxi Provincial Key Laboratory of Poultry Genetic Improvement, Institution of Biological Technology, Nanchang Normal University, Nanchang 330032, China

Received:2024-05-27 Online:2025-05-25 Published:2025-06-11

Abstract

Abstract:

This experiment aimed to investigate the protein expression profiles in testes of adult Ningdu Huang chickens, screen differentially expressed proteins and functional pathways between individuals with large and small testes, and provide foundational data for breeding selection of reproductive performance. Using testicular tissues from six 22-week-old Ningdu Huang chickens divided into large-testis(H-TES) group and small-testis(L-TES) group, tandem mass tags(TMT) technology was employed to conduct differential expression analysis, functional enrichment analysis, and gene interaction analysis of testicular proteins between the two groups. Candidate proteins were preliminarily screened, and correlations between the expression levels of these proteins in six individuals and six testicular trait indicators (left testis weight, right testis weight, total testis weight, left testis index, right testis index, total testis index) were analyzed to investigate protein functions. Results showed that 4 683 proteins were identified in Ningdu Huang chicken testes, with 144 differentially expressed proteins screened. GO analysis revealed that these differential expressed proteins primarily participate in sperm structural composition and possess functions including ubulin-glutamic acid ligase activity, thymine binding, and dehydroascorbic acid transmembrane transporter activity, etc. Significantly enriched KEGG pathways included arginine and proline metabolism, pantothenate and CoA biosynthesis, and β-alanine metabolism, etc. The protein interaction network contained 34 differential proteins, and 30 candidate proteins were preliminarily identified. Through correlation analysis and literature review, 16 key candidate proteins were screened: SPAG6, TPPP2, ENKUR, ODF2, SAXO1, TCP11, DNALI1, CCDC63, TSSK3, TEKT2, TEKT3, ALDH2, DNAH5, CCDC40, CCDC39, and DNAH10. Based on their functions, key regulatory KEGG pathways for testicular traits were identified as arginine and proline metabolism, pantothenate and CoA biosynthesis, β-alanine metabolism, tight junction, and gap junction. These findings provide fundamental data for breeding selection of testicular quality traits in local chicken breeds.

Key words: Ningdu yellow chicken, testis, tandem mass tag(TMT), proteome, candidate gene

CLC Number:

S831

MA Jing'e, WU Siqi, WAN Shumin, XIONG Xinwei, XU Jiguo, XU Jing, RAO Yousheng, ZHOU Min. Proteomic study of large and small testes in Ningdu Yellow chicken based on tandem mass tags(TMT) technology[J]. Acta Agriculturae Zhejiangensis, 2025, 37(5): 1029-1044.

Figures/Tables 9

References 49

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GO条目 GO term	GO注释号 GO ID	蛋白质注释号 Protein ID	NR注释 NR annotation	log₂FC
外动力臂组件 Outer dynein arm assembly	GO:0036158	ONT.42533.8	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.660
		ONT.34575.3	卷曲螺旋结构域蛋白63异构体X1 Coiled-coil domain?containing protein 63 isoform X1(CCDC63)	-0.716
		ONT.42533.12	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.724
		XM_040695761.2	动力蛋白重链5,轴丝样异构体X2 Dynein heavy chain 5, axonemal-like isoform X2 (DNAH5)	-0.842
精子鞭毛 Sperm flagellum	GO:0036126	ONT.31000.9	动力调节复合体亚基4 Dynein regulatory complex subunit 4 (GAS8)	-0.663
		ONT.33635.4	筑丝蛋白4 Tektin-4 (MAFIP)	-0.653
		ONT.36153.15	筑丝蛋白3 Tektin-3 (TEKT3)	-0.826
		ONT.29248.17	动力调节复合蛋白9 Dynein regulatory complex protein 9 (IQCG)	-0.685
		XM_025147182.3	精子相关抗原6 Sperm-associated antigen 6 (SPAG6)	-0.690
		ONT.44886.3	促微管聚合蛋白家族成员2 Tubulin polymerization-promoting protein family member 2 (TPPP2)	-1.394
		XM_418600.5	enkurin样蛋白Enkurin-like(ENKUR)	-0.698
		ONT.35527.13	外致密纤维蛋白2异构体X3 Outer dense fiber protein 2 isoform X3 (ODF2)	-0.646
		ONT.35594.2	精子顶体相关蛋白9异构体X1 Sperm acrosome-associated protein 9 isoform X1 (SPACA9)	-0.973
		ONT.40499.8	T复合蛋白11同源物异构体X1 T-complex protein 11 homolog isoform X1(TCP11)	-0.618
		ONT.44687.3	轴丝微管稳定因子1 Stabilizer of axonemal microtubules 1 (SAXO1)	-0.983
精子主段 Sperm principal piece	GO:0097228	XM_025147182.3	精子相关抗原6 Sperm-associated antigen 6(SPAG6)	-0.690
		ONT.33635.4	筑丝蛋白4 Tektin-4(MAFIP)	-0.653
		XM_418600.5	enkurin样蛋白Enkurin-like (ENKUR)	-0.698
外动力臂 Outer dynein arm	GO:0036157	ONT.42533.8	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.660
		ONT.42533.12	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.724
		XM_040695761.2	动力蛋白重链5,轴丝样异构体X2 Dynein heavy chain 5, axonemal-like isoform X2 (DNAH5)	-0.842
轴丝部分 Axoneme part	GO:0044447	ONT.44687.3	轴丝微管稳定因子1 Stabilizer of axonemal microtubules 1 (SAXO1)	-0.983
		ONT.42533.8	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.660
		XM_025147182.3	精子相关抗原6 Sperm-associated antigen 6(SPAG6)	-0.690
		ONT.39541.6	动力蛋白轴丝轻中间多肽1 Axonemal dynein light intermediate polypeptide 1 (DNALI1)	-0.630
内动力臂组件 Inner dynein arm assembly	GO:0036159	ONT.36702.4	卷曲螺旋结构域蛋白40 Coiled-coil domain?containing protein 40(CCDC40)	-0.646
		ONT.28739.10	卷曲螺旋结构域蛋白39 Coiled-coil domain?containing protein 39(CCDC39)	-0.742
		ONT.39541.6	动力蛋白轴丝轻中间多肽1 Axonemal dynein light intermediate polypeptide 1 (DNALI1)	-0.630
		ONT.39554.2	筑丝蛋白2 Tektin-2(TEKT2)	-0.710

GO条目 GO term	GO注释号 GO ID	蛋白质注释号 Protein ID	NR注释 NR annotation	log₂FC
外动力臂组件 Outer dynein arm assembly	GO:0036158	ONT.42533.8	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.660
		ONT.34575.3	卷曲螺旋结构域蛋白63异构体X1 Coiled-coil domain?containing protein 63 isoform X1(CCDC63)	-0.716
		ONT.42533.12	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.724
		XM_040695761.2	动力蛋白重链5,轴丝样异构体X2 Dynein heavy chain 5, axonemal-like isoform X2 (DNAH5)	-0.842
精子鞭毛 Sperm flagellum	GO:0036126	ONT.31000.9	动力调节复合体亚基4 Dynein regulatory complex subunit 4 (GAS8)	-0.663
		ONT.33635.4	筑丝蛋白4 Tektin-4 (MAFIP)	-0.653
		ONT.36153.15	筑丝蛋白3 Tektin-3 (TEKT3)	-0.826
		ONT.29248.17	动力调节复合蛋白9 Dynein regulatory complex protein 9 (IQCG)	-0.685
		XM_025147182.3	精子相关抗原6 Sperm-associated antigen 6 (SPAG6)	-0.690
		ONT.44886.3	促微管聚合蛋白家族成员2 Tubulin polymerization-promoting protein family member 2 (TPPP2)	-1.394
		XM_418600.5	enkurin样蛋白Enkurin-like(ENKUR)	-0.698
		ONT.35527.13	外致密纤维蛋白2异构体X3 Outer dense fiber protein 2 isoform X3 (ODF2)	-0.646
		ONT.35594.2	精子顶体相关蛋白9异构体X1 Sperm acrosome-associated protein 9 isoform X1 (SPACA9)	-0.973
		ONT.40499.8	T复合蛋白11同源物异构体X1 T-complex protein 11 homolog isoform X1(TCP11)	-0.618
		ONT.44687.3	轴丝微管稳定因子1 Stabilizer of axonemal microtubules 1 (SAXO1)	-0.983
精子主段 Sperm principal piece	GO:0097228	XM_025147182.3	精子相关抗原6 Sperm-associated antigen 6(SPAG6)	-0.690
		ONT.33635.4	筑丝蛋白4 Tektin-4(MAFIP)	-0.653
		XM_418600.5	enkurin样蛋白Enkurin-like (ENKUR)	-0.698
外动力臂 Outer dynein arm	GO:0036157	ONT.42533.8	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.660
		ONT.42533.12	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.724
		XM_040695761.2	动力蛋白重链5,轴丝样异构体X2 Dynein heavy chain 5, axonemal-like isoform X2 (DNAH5)	-0.842
轴丝部分 Axoneme part	GO:0044447	ONT.44687.3	轴丝微管稳定因子1 Stabilizer of axonemal microtubules 1 (SAXO1)	-0.983
		ONT.42533.8	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1 (DNAI1)	-0.660
		XM_025147182.3	精子相关抗原6 Sperm-associated antigen 6(SPAG6)	-0.690
		ONT.39541.6	动力蛋白轴丝轻中间多肽1 Axonemal dynein light intermediate polypeptide 1 (DNALI1)	-0.630
内动力臂组件 Inner dynein arm assembly	GO:0036159	ONT.36702.4	卷曲螺旋结构域蛋白40 Coiled-coil domain?containing protein 40(CCDC40)	-0.646
		ONT.28739.10	卷曲螺旋结构域蛋白39 Coiled-coil domain?containing protein 39(CCDC39)	-0.742
		ONT.39541.6	动力蛋白轴丝轻中间多肽1 Axonemal dynein light intermediate polypeptide 1 (DNALI1)	-0.630
		ONT.39554.2	筑丝蛋白2 Tektin-2(TEKT2)	-0.710

KEGG注释号 KEGG ID	信号通路名称 Signal pathway name	蛋白质注释号 Protein ID	NR注释 NR annotation	log₂FC
ko00770	泛酸和辅酶A生物合成 Pantothenate and CoA biosynthesis	NM_001277426.2	二氢嘧啶酶Dihydropyrimidinase(DPYS)	-1.113
ko00770	泛酸和辅酶A生物合成 Pantothenate and CoA biosynthesis	ONT.34582.1	醛脱氢酶,线粒体异构体X3 Aldehyde dehydrogenase, mitochondrial isoform X3 (ALDH2)	0.847
ko00410	β-丙氨酸代谢 β-Alanine metabolism	ONT.34582.1	醛脱氢酶,线粒体异构体X3 Aldehyde dehydrogenase, mitochondrial isoform X3 (ALDH2)	0.847
ko00410	β-丙氨酸代谢 β-Alanine metabolism	NM_001277426.2	二氢嘧啶酶Dihydropyrimidinase(DPYS)	-1.113
ko00330	精氨酸和脯氨酸代谢 Arginine and proline metabolism	NM_205310.2	肌酸激酶,睾丸同工酶 Creatine kinase, testis isozyme(CKB)	-0.76
		ONT.45247.3	线粒体S型肌酸激酶 Creatine kinase S-type, mitochondrial(CKMT2)	-0.814
		XM_046941482.1	肌酸激酶,睾丸同工酶 Creatine kinase, testis isozyme (CKB)	-0.709
		ONT.34582.1	醛脱氢酶,线粒体异构体X3 Aldehyde dehydrogenase, mitochondrial isoform X3 (ALDH2)	0.847

KEGG注释号 KEGG ID	信号通路名称 Signal pathway name	蛋白质注释号 Protein ID	NR注释 NR annotation	log₂FC
ko00770	泛酸和辅酶A生物合成 Pantothenate and CoA biosynthesis	NM_001277426.2	二氢嘧啶酶Dihydropyrimidinase(DPYS)	-1.113
ko00770	泛酸和辅酶A生物合成 Pantothenate and CoA biosynthesis	ONT.34582.1	醛脱氢酶,线粒体异构体X3 Aldehyde dehydrogenase, mitochondrial isoform X3 (ALDH2)	0.847
ko00410	β-丙氨酸代谢 β-Alanine metabolism	ONT.34582.1	醛脱氢酶,线粒体异构体X3 Aldehyde dehydrogenase, mitochondrial isoform X3 (ALDH2)	0.847
ko00410	β-丙氨酸代谢 β-Alanine metabolism	NM_001277426.2	二氢嘧啶酶Dihydropyrimidinase(DPYS)	-1.113
ko00330	精氨酸和脯氨酸代谢 Arginine and proline metabolism	NM_205310.2	肌酸激酶,睾丸同工酶 Creatine kinase, testis isozyme(CKB)	-0.76
		ONT.45247.3	线粒体S型肌酸激酶 Creatine kinase S-type, mitochondrial(CKMT2)	-0.814
		XM_046941482.1	肌酸激酶,睾丸同工酶 Creatine kinase, testis isozyme (CKB)	-0.709
		ONT.34582.1	醛脱氢酶,线粒体异构体X3 Aldehyde dehydrogenase, mitochondrial isoform X3 (ALDH2)	0.847

蛋白质ID Protein ID	KEGG信号通路 KEGG signal pathway	NR注释 NR annotation	log₂FC
ONT.42533.8	—	动力蛋白中链1,轴丝异构体X1 Dynein intermediate chain 1, axonemal isoform X1(DNAI1)	-0.660
ONT.39541.6	—	动力蛋白轴丝轻中间多肽1 Axonemal dynein light intermediate polypeptide 1(DNALI1)	-0.630
ONT.34575.3	—
ONT.34953.4	—	轴丝动力蛋白重链10 Dynein heavy chain 10, axonemal (DNAH10)	-0.590
XM_040695761.2	—	动力蛋白重链5,轴丝样异构体X2 Dynein heavy chain 5, axonemal-like isoform X2 (DNAH5)	-0.842
ONT.1292.4	吞噬体Phagosome (ko04145) 细胞凋亡Apoptosis (ko04210) 紧密连接Tight junction (ko04530) 间隙连接Gap junction (ko04540)	α-微管蛋白2链 Tubulin alpha-2 chain(TUBA8B)	-0.924
ONT.39373.1	—	睾丸特异性丝/苏氨酸蛋白激酶3 Testis-specific serine/threonine-protein kinase 3(TSSK3)	-0.805
XM_426278.5	—	假设蛋白RvY_17884 Hypothetical protein RvY_17884(LOC428720)	-1.293
ONT.40848.2	心脏肌肉收缩 Cardiac muscle contraction (ko04260) 心肌细胞肾上腺素能信号传导 Adrenergic signaling in cardiomyocytes (ko04261) Apelin信号通路 Apelin signaling pathway (ko04371)	肌球蛋白轻链4 Myosin light chain 4 (MYL4)	-0.587
ONT.36865.19	—	钙/钙调蛋白依赖性蛋白激酶激酶1异构体X2 Calcium/calmodulin-dependent protein kinase kinase 1 isoform X2 (CAMKK1)	-0.587

Proteomic study of large and small testes in Ningdu Yellow chicken based on tandem mass tags(TMT) technology

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蛋白质注释号 Protein ID	log₂FC	基因名称 Gene name	屠宰活重 Slaughter weight	左睾丸重 Left testis weight	右睾丸重 Right testis weight	睾丸总重 Total testis weight	左睾丸率 Left testis percentage	右睾丸率 Right testis percentage	总睾丸率 Total testis percentage
ONT.42533.8	-0.660	DNAI1	0.836^*	0.929^**	0.931^**	0.947^**	0.891^*	0.848^*	0.883^*
ONT.42533.12	-0.724	DNAI1	0.862^*	0.947^**	0.948^**	0.965^**	0.912^*	0.868^*	0.904^*
ONT.34575.3	-0.716	CCDC63	0.778	0.927^**	0.984^**	0.973^**	0.924^**	0.933^**	0.944^**
XM_040695761.2	-0.842	DNAH5	0.889^*	0.955^**	0.896^*	0.943^**	0.903^*	0.803	0.864^*
ONT.31000.9	-0.663	GAS8	0.831^*	0.948^**	0.967^**	0.975^**	0.926^**	0.899^*	0.927^**
ONT.33635.4	-0.653	MAFIP	0.843^*	0.968^**	0.956^**	0.980^**	0.940^**	0.884^*	0.926^**
ONT.36153.15	-0.826	TEKT3	0.783	0.879^*	0.953^**	0.933^**	0.863^*	0.889^*	0.891^*
ONT.29248.17	-0.685	IQCG	0.863^*	0.928^**	0.935^**	0.949^**	0.888^*	0.851^*	0.883^*
XM_025147182.3	-0.690	SPAG6	0.698	0.828^*	0.942^**	0.902^*	0.829^*	0.895^*	0.878^*
ONT.44886.3	-1.394	TPPP2	0.756	0.907^*	0.970^**	0.956^**	0.901^*	0.916^*	0.924^**
XM_418600.5	-0.698	ENKUR	0.810	0.903^*	0.943^**	0.940^**	0.875^*	0.868^*	0.886^*
ONT.35527.13	-0.646	ODF2	0.688	0.938^**	0.997^**	0.985^**	0.964^**	0.976^**	0.987^**
ONT.35594.2	-0.973	SPACA9	0.852^*	0.954^**	0.925^**	0.957^**	0.912^*	0.839^*	0.888^*
ONT.40499.8	-0.618	TCP11	0.806	0.960^**	0.902^*	0.948^**	0.924^**	0.827^*	0.888^*
ONT.44687.3	-0.983	SAXO1	0.831^*	0.934^**	0.951^**	0.960^**	0.908^*	0.880^*	0.908^*
ONT.39541.6	-0.630	DNALI1	0.786	0.901^*	0.966^**	0.951^**	0.892^*	0.910^*	0.916^*
ONT.36702.4	-0.646	CCDC40	0.908^*	0.907^*	0.889^*	0.914^*	0.849^*	0.789	0.831^*
ONT.28739.10	-0.742	CCDC39	0.878^*	0.944^**	0.849^*	0.912^*	0.877^*	0.744	0.820^*
ONT.39554.2	-0.710	TEKT2	0.806	0.905^*	0.961^**	0.951^**	0.888^*	0.896^*	0.907^*
NM_001277426.2	-1.113	DPYS	0.735	0.899^*	0.981^**	0.958^**	0.905^*	0.939^**	0.938^**
ONT.34582.1	0.847	ALDH2	-0.708	-0.942^**	-0.988^**	-0.983^**	-0.965^**	-0.965^**	-0.981^**
NM_205310.2	-0.760	CKB	0.837^*	0.912^*	0.932^**	0.939^**	0.875^*	0.849^*	0.876^*
XM_046941482.1	-0.709	CKB	0.873^*	0.883^*	0.856^*	0.885^*	0.815^*	0.746	0.792
ONT.45247.3	-0.814	CKMT2	0.742	0.912^*	0.988^**	0.968^**	0.920^**	0.947^**	0.949^**
ONT.34953.4	-0.590	DNAH10	0.633	0.782	0.946^**	0.880^*	0.822^*	0.937^**	0.897^*
ONT.1292.4	-0.924	TUBA8B	0.784	0.952^**	0.972^**	0.980^**	0.939^**	0.913^*	0.941^**
ONT.39373.1	-0.805	TSSK3	0.830^*	0.889^*	0.944^**	0.933^**	0.865^*	0.874^*	0.884^*
XM_426278.5	-1.293	LOC428720	0.648	0.893^*	0.994^**	0.961^**	0.927^**	0.980^**	0.971^**
ONT.40848.2	-0.587	MYL4	0.947^**	0.919^**	0.766	0.857^*	0.836^*	0.653	0.752
ONT.36865.19	-0.587	CAMKK1	0.884^*	0.956^**	0.945^**	0.968^**	0.923^**	0.869^*	0.910^*

基因名称 Gene name	log₂FC	功能 Function
SPAG6	-0.690	调节精子活力,调控精子顶体形成,影响精子发生 Regulation of sperm motility and sperm acrosome formation, influencing on spermatogenesis
TPPP2	-1.394	与精子线粒体结构和功能相关,影响精子数量、活力以及生育能力Correlating with sperm mitochondrial structure and function, affecting sperm count, viability, and fertility
ENKUR	-0.698	调节鞭毛的弯曲Regulation of flagellar curvature
ODF2	-0.646	调节精子活力Regulation of sperm motility
SAXO1	-0.983	可能在精子鞭毛发生、稳定性和长度方面起着关键作用 May play a key role in the biogenesis, stability and length of the sperm flagellum
TCP11	-0.618	影响精子活力Influencing on sperm motility
DNALI1	-0.630	参与精子发育和精子鞭毛正确组装Involved in sperm development and correct assembly of the sperm flagellum
CCDC63	-0.716	敲除会因鞭毛缩短导致雄性小鼠不育Knockout causes sterility in male mice due to flagellar shortening
CCDC39	-0.742	在精子鞭毛中相互作用,影响雄性生育能力Interacting in the sperm flagellum and affecting male fertility
CCDC40	-0.646
DNAH10	-0.590	缺失会导致精子鞭毛形态异常Deficiency leads to abnormal sperm flagellar morphology
DNAH5	-0.842	与精子活力和形态有关Related to sperm motility and morphology
TSSK3	-0.805	精子形态发生和雄性维持生育能力所必需,影响精子形成 Essential for sperm morphogenesis and for male maintenance of fertility, affecting sperm formation
TEKT2	-0.710	作为鞭毛稳定性或精子活力所需的外致密纤维附属分子发挥作用 Playing a role as an outer dense fiber accessory molecule required for flagellar stability or sperm motility
TEKT3	-0.826	对鞭毛稳定性以及精子活力起作用,参与顶体相关事件 Playing a role in flagellar stability and sperm motility, participation in acrosome-related events
ALDH2	0.847	抗细胞凋亡Antiapoptotic

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