Molecular characterization and genetic evolutionary analysis of hemagglutinin gene of five H9N2 subtype avian influenza viruses in Zhejiang Province, China

doi:10.3969/j.issn.1004-1524.20250359

Acta Agriculturae Zhejiangensis ›› 2025, Vol. 37 ›› Issue (12): 2494-2503.DOI: 10.3969/j.issn.1004-1524.20250359

• Animal Science • Previous Articles Next Articles

Molecular characterization and genetic evolutionary analysis of hemagglutinin gene of five H9N2 subtype avian influenza viruses in Zhejiang Province, China

LIU Shizhe¹^,²(), HUA Jionggang², CHEN Liu², XIE Ronghui³, YE Weicheng², ZHANG Chuanliang³, ZHU Yinchu², FENG Xiaoxiao³, FU Yuan², NI Zheng², ZHANG Cun², QU Yonggang¹^,^*(), YUN Tao²^,^*()

1. College of Animal Science and Technology, Shihezi University, Shihezi 832003, Xinjiang, China
2. Zhejiang Key Laboratory of Livestock and Poultry Biotech Breeding, Key Laboratory of Livestock and Poultry Resources (Poultry) Evaluation and Utilization, Ministry of Agriculture and Rural Affairs, Zhejiang Engineering Research Center for Poultry Breeding Industry and Green Farming Technology, Institute of Animal Husbandry and Veterinary Sciences, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
3. Zhejiang Center of Animal Disease Control and Prevention, Hangzhou 311199, China

Received:2025-05-06 Online:2025-12-25 Published:2026-01-09

Abstract

Abstract:

Avian influenza virus (AIV) subtype H9N2 is the most prevalent low pathogenic avian influenza (LPAIV) in avian species in China, posing a serious threat to the farming industry and public health safety due to its persistent antigenic drift and the risk of cross-species transmission. In order to understand the genetic evolutionary characteristics of H9N2 subtype AIV prevalent in Zhejiang Province, the present study was conducted to determine the gene sequence and molecular characterization of the hemagglutinin (HA) gene of five locally isolated H9N2 subtype AIV strains. The results showed that the five isolates belonged to the h9.4.2.1 and h9.4.2.5 branches of the Eurasian lineage, and the nucleotide and amino acid homologies of the HA gene ranged from 83.51% to 99.88% and 86.33% to 99.83%, respectively. Notably, the isolates A/Chicken/Zhejiang/HZ01/2022 and A/Duck/Zhejiang/TZ01/2022 showed only 88.24%-88.35% nucleotide homology and 89.43%-90.82% amino acid homology of HA gene with the vaccine strain CK/SS/94. The HA cleavage sites of all isolates were characterized by single basic amino acid, which was consistent with the characteristics of low pathogenicity virus. Receptor binding site analysis revealed mutations I163T, H191N, A198T/V, Q234L, and Q235M, which might enhance the binding ability of the virus to the human sialic acid α-2,6-galactose receptor. Glycosylation site analysis revealed the presence of 7-8 potential glycosylation sites in the isolates, with deletions at sites 218 and 551 and additions at sites 206 and 313, and these mutations may enhance viral adaptation to mammalian hosts. In addition, HA protein antigenic sites were present with mutations at 234, 285 and 334, while sites 181, 280, 281 and 296 were highly conserved. The study suggests that Zhejiang Province H9N2 subtype AIV continues to evolve through mutations at key sites and altered glycosylation patterns, which may lead to enhanced virulence, decreased vaccine protection efficacy, and increased risk of cross-species transmission. There is an urgent need to strengthen the molecular surveillance of local endemic strains and optimize the vaccine strain match to enhance the control efficacy and reduce the public health threat.

Key words: Avian influenza virus, H9N2 subtype, HA gene, genetic evolution, genetic analysis

CLC Number:

S855.3

LIU Shizhe, HUA Jionggang, CHEN Liu, XIE Ronghui, YE Weicheng, ZHANG Chuanliang, ZHU Yinchu, FENG Xiaoxiao, FU Yuan, NI Zheng, ZHANG Cun, QU Yonggang, YUN Tao. Molecular characterization and genetic evolutionary analysis of hemagglutinin gene of five H9N2 subtype avian influenza viruses in Zhejiang Province, China[J]. Acta Agriculturae Zhejiangensis, 2025, 37(12): 2494-2503.

Figures/Tables 8

References 14

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序号 Number	参考毒株 Reference strain	缩写 Abbreviation	HA基因登录号 Accession number
1	A/Turkey/Wisconsin/1/1966	TK/1/66	CY130054.1
2	A/Chicken/Shanghai/F/98	CK/F/98	AY743216.1
3	A/Chicken/Beijing/1/94	CK/1/94	AF156380.1
4	A/Chicken/Guangdong/SS/94	CK/SS/94	AF384557
5	A/Duck/Hong Kong/Y280/97	DK/Y280/97	AF156376.1
6	A/Turkey/California/189/66	TK/189/66	AF156390.1
7	A/Shorebird/Delaware/9/96	SB/9/96	AF156386.1
8	A/Chicken/Korea/SH0802/2008	CK/SH/08	HQ221677.1
9	A/Chicken/Korea/MS96-CE6/1996	CK/MS/96	GU053186.1
10	A/Chicken/Israel/178/2006	CK/178/06	EF492224.1
11	A/Chicken/Karaj/GHA/2017	CK/GHA/17	MH360730.1
12	A/Chicken/Henan/43/02	CK/43/02	DQ064369.1
13	A/Goose/China/JY100405/2018	GS/JY/18	OQ804402.1
14	A/Chicken/Jiangsu/J2303/2018	CK/J2303/18	MK553246.1
15	A/Chicken/Rizhao/1436/2013	CK/1436/13	KF259177.1
16	A/Chicken/China/GD2021/2021	CK/GD2021/21	MW548848.1
17	A/Chicken/Daye/DY0602/2017	CK/DY0602/17	MF794999.1
18	A/Chicken/China/355/2017	CK/355/17	MN385379.1
19	A/Chicken/Guangzhou/18/2019	CK/18/19	OQ054042.1
20	A/Chicken/China/D3/2022	CK/D3/22	OR528233.1
21	A/Duck/Guangdong/FS91/2022	DK/FS91/22	OQ826094.1
22	A/Environment/Xiamen/01/2021	EN/01/21	ON856628.1
23	A/Chicken/Shandong/6/96	CK/6/96	DQ064376.1
24	A/Chicken/Shandong/1/2000	CK/1/00	FJ793404.1
25	A/Chicken/Jilin/A/2012	CK/A/12	KF886521.1
26	A/Chicken/Jiangxi/X1459/2018	CK/X1459/18	MK552958.1
27	A/Chicken/Guizhou/B11/2011	CK/B11/11	JN804200.1
28	A/Chicken/Guangdong/WBQ02/2012	CK/WB/12	KJ768997.1

序号 Number	参考毒株 Reference strain	缩写 Abbreviation	HA基因登录号 Accession number
1	A/Turkey/Wisconsin/1/1966	TK/1/66	CY130054.1
2	A/Chicken/Shanghai/F/98	CK/F/98	AY743216.1
3	A/Chicken/Beijing/1/94	CK/1/94	AF156380.1
4	A/Chicken/Guangdong/SS/94	CK/SS/94	AF384557
5	A/Duck/Hong Kong/Y280/97	DK/Y280/97	AF156376.1
6	A/Turkey/California/189/66	TK/189/66	AF156390.1
7	A/Shorebird/Delaware/9/96	SB/9/96	AF156386.1
8	A/Chicken/Korea/SH0802/2008	CK/SH/08	HQ221677.1
9	A/Chicken/Korea/MS96-CE6/1996	CK/MS/96	GU053186.1
10	A/Chicken/Israel/178/2006	CK/178/06	EF492224.1
11	A/Chicken/Karaj/GHA/2017	CK/GHA/17	MH360730.1
12	A/Chicken/Henan/43/02	CK/43/02	DQ064369.1
13	A/Goose/China/JY100405/2018	GS/JY/18	OQ804402.1
14	A/Chicken/Jiangsu/J2303/2018	CK/J2303/18	MK553246.1
15	A/Chicken/Rizhao/1436/2013	CK/1436/13	KF259177.1
16	A/Chicken/China/GD2021/2021	CK/GD2021/21	MW548848.1
17	A/Chicken/Daye/DY0602/2017	CK/DY0602/17	MF794999.1
18	A/Chicken/China/355/2017	CK/355/17	MN385379.1
19	A/Chicken/Guangzhou/18/2019	CK/18/19	OQ054042.1
20	A/Chicken/China/D3/2022	CK/D3/22	OR528233.1
21	A/Duck/Guangdong/FS91/2022	DK/FS91/22	OQ826094.1
22	A/Environment/Xiamen/01/2021	EN/01/21	ON856628.1
23	A/Chicken/Shandong/6/96	CK/6/96	DQ064376.1
24	A/Chicken/Shandong/1/2000	CK/1/00	FJ793404.1
25	A/Chicken/Jilin/A/2012	CK/A/12	KF886521.1
26	A/Chicken/Jiangxi/X1459/2018	CK/X1459/18	MK552958.1
27	A/Chicken/Guizhou/B11/2011	CK/B11/11	JN804200.1
28	A/Chicken/Guangdong/WBQ02/2012	CK/WB/12	KJ768997.1

毒株 Strain	分离时间 Time	地区 Area	宿主 Specie	基因 Gene	同源性最高的病毒株 Viral strain with the highest homology	核酸同源性 Nucleotide homology/%	氨基酸同源性 Amino acid homology/%	登录号 Accession number
A/Chicken/Zhejiang/ HZ01/2022 (CK/01/22)	2022	杭州 Hangzhou	鸡 Gallus demesticus	HA	A/Chicken/Jiangxi/ X1459/2018(H9N2)	98.75	99.29	MK552958.1
A/Quails/Zhejiang/ SY01/2012 (QU/01/12)	2012	上虞 Shangyu	鹌鹑 Coturnix japonica	HA	A/Chicken/Shanghai/ S2277/2017(H9N2)	98.70	97.39	MK554249.1
A/Quails/Zhejiang/ JX535/2012 (QU/535/12)	2012	嘉兴 Jiaxing	鹌鹑 Coturnix japonica	HA	A/Chicken/Shanghai/ S2277/2017(H9N2)	98.88	98.32	MK554249.1
A/Chicken/Zhejiang/ XS541/2018 (CK/541/18)	2018	象山 Xiangshan	鸡 Gallus demesticus	HA	A/Chicken/Jilin/ A/2012(H9N2)	99.81	99.44	KF886521.1
A/Duck/Zhejiang/ TZ01/2022 (DK/01/22)	2022	台州 Taizhu	鸭 Anas platyrhynchos	HA	A/Chicken/Jiangxi/ X1459/2018(H9N2)	99.75	99.29	MK552958.1

毒株 Strain	分离时间 Time	地区 Area	宿主 Specie	基因 Gene	同源性最高的病毒株 Viral strain with the highest homology	核酸同源性 Nucleotide homology/%	氨基酸同源性 Amino acid homology/%	登录号 Accession number
A/Chicken/Zhejiang/ HZ01/2022 (CK/01/22)	2022	杭州 Hangzhou	鸡 Gallus demesticus	HA	A/Chicken/Jiangxi/ X1459/2018(H9N2)	98.75	99.29	MK552958.1
A/Quails/Zhejiang/ SY01/2012 (QU/01/12)	2012	上虞 Shangyu	鹌鹑 Coturnix japonica	HA	A/Chicken/Shanghai/ S2277/2017(H9N2)	98.70	97.39	MK554249.1
A/Quails/Zhejiang/ JX535/2012 (QU/535/12)	2012	嘉兴 Jiaxing	鹌鹑 Coturnix japonica	HA	A/Chicken/Shanghai/ S2277/2017(H9N2)	98.88	98.32	MK554249.1
A/Chicken/Zhejiang/ XS541/2018 (CK/541/18)	2018	象山 Xiangshan	鸡 Gallus demesticus	HA	A/Chicken/Jilin/ A/2012(H9N2)	99.81	99.44	KF886521.1
A/Duck/Zhejiang/ TZ01/2022 (DK/01/22)	2022	台州 Taizhu	鸭 Anas platyrhynchos	HA	A/Chicken/Jiangxi/ X1459/2018(H9N2)	99.75	99.29	MK552958.1

毒株 Strain	核苷酸同源性Nucleotide homology				氨基酸同源性Amino acid homology
毒株 Strain	CK/SS/94	CK/F/98	CK/6/96	CK/1/00	CK/SS/94	CK/F/98	CK/6/96	CK/1/00
CK/01/22	88.35	87.88	87.70	87.44	90.18	90.18	89.64	89.62
QU/01/12	87.84	86.60	86.78	86.78	89.70	88.39	88.80	88.53
QU/535/12	88.46	87.21	88.08	87.41	90.82	89.14	89.57	89.83
CK/541/18	96.12	94.67	95.49	94.88	97.56	96.80	96.43	96.35
DK/01/22	88.24	87.76	87.58	87.31	90.00	90.00	89.46	89.43

Molecular characterization and genetic evolutionary analysis of hemagglutinin gene of five H9N2 subtype avian influenza viruses in Zhejiang Province, China

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分离株 Strain	裂解位点 Cleavage site	左侧臂 Left side wall	右侧臂 Right side wall	受体结合位点 Receptor binding site
分离株 Strain	333-341	232-237	146-150	109	161	163	191	198	202	203	224
CK/GHA/17*	PARSSR↓GLF	NGLIGR	GTSKS	Y	W	T	H	A	L	Y	L
CK/BJ/94*	PARSSR↓GLF	NGQQGR	GTSKA	Y	W	T	N	V	L	Y	Q
CK/F/98*	PARSSR↓GLF	NGQQGR	GTSKA	Y	W	T	N	A	L	Y	Q
CK/SS/94*	PAGSSR↓GLF	NGQQGR	GTSKA	Y	W	T	N	A	L	Y	V
DK/Y280/97*	PARSSR↓GLF	NGLQGR	GTSKA	Y	W	T	N	T	L	Y	L
CK/43/02*	PARSSR↓GLF	NGLQGR	GTSRA	Y	W	T	N	A	L	Y	L
EN/01/2021*	PSRSSR↓GLF	NGLMGR	GTSNT	Y	W	N	N	V	L	Y	L
CK/D3/2022*	PSRSSR↓GLF	NGLMGR	GTSKT	Y	W	N	N	V	L	Y	L
CK/01/22	PSRSSR↓GLF	NGLMGR	GTSTA	Y	W	T	N	T	L	Y	L
QU/01/12	PARSSR↓GLF	NGQQGR	GTSIS	Y	W	T	H	A	L	Y	V
QU/535/12	PARSSR↓GLF	NGQQGR	GTSIS	Y	W	T	H	T	L	Y	V
CK/541/18	PARLSR↓GLF	NGQQGR	GTSKA	Y	W	T	N	T	L	Y	L
DK/01/22	PSRSSR↓GLF	NGLMGR	GTSTA	Y	W	T	N	T	L	Y	L

分离株 Strain	糖基化位点Glycosylation site
分离株 Strain	29	82	141	206	218	298	305	313	492	551
CK/GHA/17*	NSTE	NPSC	NVTY			NSTL	NISK		NGTY	NGSC
CK/BJ/94*	NSTE	NPSC	NVTY		NRTF	NTTL	NVSK		NGTY	NGSC
CK/F/98*	NSTE	NPSC	NVSY			NTTL	NVSK		NGTY	NGSC
CK/SS/94*	NSTE	NPSC	NVSY		NRTF	NTTL	NVSK		NGTY	NGSC
Dk/Y280/97*	NSTE	NPSC	NVSY		NRTF	NTTL	NVSK		NGTY
CK/43/02*	NSTE	NPSC	NVSY		NRTF	NTTL	NVSK		NGTY	NGSC
EN/01/2021*	NSTE	NPSC	NVSY			NTTL	NVSK	NCSK	NGTY	NGSC
CK/D3/2022*	NSTE	NPSC	NVSY			NTTL	NVSK	NCSK	NGTY	NGSC
CK/01/22	NSTE	NPSC	NVSY			NTTL	NVSK	NCSK	NGTY	NGSC
QU/01/12	NSTE	NPSC	NVSY	NDTT	NRTF	NSTL	NISK		NGTY
QU/535/12	NSTE	NPSC	NVSY	NDTT	NRTF	NSTL	NISK		NGTY
CK/541/18	NSTE	NPSC	NVSY		NRTF	NTTL	NVSK		NGTY
DK/01/22	NSTE	NPSC	NVSY			NTTL	NVSK	NCSK	NGTY	NGSC

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