豆科作物AOX基因鉴定及其在普通菜豆响应非生物胁迫中的表达模式研究

doi:10.3724/SP.J.1006.2025.44170

作物学报 ›› 2025, Vol. 51 ›› Issue (7): 1769-1783.doi: 10.3724/SP.J.1006.2025.44170

• 作物遗传育种·种质资源·分子遗传学 • 上一篇下一篇

豆科作物AOX基因鉴定及其在普通菜豆响应非生物胁迫中的表达模式研究

闫知兰¹(), 赵芹¹, 常甜达¹, 王一鸣¹, 王碧辉¹, 王鹏¹, 黄春国¹, 张会², 王利祥¹, 郝晓鹏³^,^*(), 赵波¹^,^*()

¹山西农业大学农学院 / 山西省后稷实验室, 山西太原 030031
²山西农业大学生命科学学院, 山西太谷 030801
³山西农业大学农业基因资源研究中心 / 杂粮种质资源发掘与遗传改良山西省重点实验室, 山西太原 030031

收稿日期:2024-10-06 接受日期:2025-04-27 出版日期:2025-07-12 网络出版日期:2025-05-13
通讯作者: *赵波, E-mail: bozhao2022@sxau.edu.cn; 郝晓鹏, E-mail: hxp9802@163.com
作者简介:E-mail: 1795857816@qq.com
基金资助:
国家重点研发计划项目(2023YFD1202700);国家重点研发计划项目(2023YFD1202703);国家自然科学基金项目(32301778);博士后研究人员来晋工作奖励经费科研项目(SXBYKY2023004);山西省基础研究计划(自由探索类)项目(202403021211051);山西省基础研究计划(自由探索类)项目(202203021222147);山西省后稷实验室自主立项课题(202304010930003-03);山西省科技创新人才团队专项(202204051002013)

Genome-wide identification and characterization of Alternative oxidase (AOX) genes in leguminous crops and their expression patterns in response to abiotic stresses in common bean

YAN Zhi-Lan¹(), ZHAO Qin¹, CHANG Tian-Da¹, WANG Yi-Ming¹, WANG Bi-Hui¹, WANG Peng¹, HUANG Chun-Guo¹, ZHANG Hui², WANG Li-Xiang¹, HAO Xiao-Peng³^,^*(), ZHAO Bo¹^,^*()

¹College of Agriculture, Shanxi Agricultural University / Shanxi Houji Laboratory, Taiyuan 030031, Shanxi, China
²College of Life Sciences, Shanxi Agricultural University, Taigu 030801, Shanxi, China
³Agricultural Gene Resources Research Center, Shanxi Agricultural University / Key Laboratory of Germplasm Resources Exploration and Genetic Improvement of Coarse Cereals, Taiyuan 030031, Shanxi, China

Received:2024-10-06 Accepted:2025-04-27 Published:2025-07-12 Published online:2025-05-13
Contact: *E-mail: bozhao2022@sxau.edu.cn; E-mail: hxp9802@163.com
Supported by:
National Key R&D Program of China(2023YFD1202700);National Key R&D Program of China(2023YFD1202703);National Natural Science Foundation of China(32301778);Shanxi Province’s Reward Fund for Doctoral Graduates and Postdoctoral Researchers to Work in Shanxi Province(SXBYKY2023004);Shanxi Provincial Basic Research Program-free Exploration Category(202403021211051);Shanxi Provincial Basic Research Program-free Exploration Category(202203021222147);Shanxi Houji Laboratory Self-initiated Research Projects(202304010930003-03);Special Fund for Science and Technology Innovation Teams of Shanxi Province(202204051002013)

摘要/Abstract

摘要：

交替氧化酶(alternative oxidase, AOX)是一种重要的线粒体末端氧化酶, 在植物抵御非生物胁迫中扮演着关键角色。豆科作物作为植物蛋白的重要来源, 在农业可持续发展中发挥着重要作用。然而, 近年来频发的极端气候对豆科作物的产量和品质造成了严重影响, 提高其耐逆性已成为亟待解决的问题。本研究对大豆、普通菜豆、宽叶菜豆和绿豆4种豆科作物的AOX基因家族进行了系统性的鉴定和分析, 包括蛋白结构、理化性质、启动子顺式作用元件, 以及普通菜豆AOX基因在多种非生物胁迫下的表达模式。家族成员鉴定发现, 大豆、普通菜豆、宽叶菜豆和绿豆分别包含4个、3个、3个和3个AOX基因, 亲缘关系分析将其划分为3个不同的亚族。顺式作用元件分析结果显示, 豆科作物AOX基因启动子区域存在很多响应激素和逆境胁迫的顺式作用元件。对普通菜豆AOX基因在不同非生物胁迫下的表达模式进行分析发现, 其AOX同源基因对不同非生物胁迫刺激响应存在差异, 表现出多样的时序变化模式。其中, PvAOX1A;2受多种非生物胁迫的诱导显著上调表达。而PvAOX2;2_2受盐胁迫和高温胁迫诱导显著上调表达, PvAOX2;2_1受冷胁迫诱导显著上调表达。综上, 普通菜豆AOX基因可能在其应答非生物胁迫中发挥着重要作用。本研究相关结果不仅为深入探究豆科作物AOX基因的生物学功能提供了重要线索, 也为普通菜豆耐逆性的分子改良提供了潜在的靶基因。

关键词: 普通菜豆, AOX, 豆科作物, 非生物胁迫, 表达模式

Abstract:

Alternative oxidase (AOX), a key terminal oxidase in the mitochondrial electron transport chain, plays a pivotal role in plant response to various abiotic stresses. Leguminous crops are not only important sources of plant-based protein but also contribute significantly to sustainable agricultural development. However, their yield and quality have been increasingly compromised by frequent extreme climatic events, highlighting the urgent need to enhance their stress tolerance. In this study, we systematically identified and analyzed the AOX gene family in four leguminous crops: soybean, common bean, tepary bean, and mung bean. Our analysis included assessments of protein structure, physicochemical properties, promoter cis-acting elements, and the expression patterns of AOX genes in common bean under different abiotic stress treatments. We identified four, three, three, and three AOX genes in soybean, common bean, tepary bean, and mung bean, respectively. Phylogenetic analysis grouped these genes into three distinct subfamilies. Cis-element analysis of promoter regions revealed an abundance of hormone-responsive and stress-responsive elements. Expression profiling in common bean demonstrated that AOX genes exhibit differential responses to various abiotic stresses, with distinct temporal expression patterns. Notably, PvAOX1A;2 was strongly upregulated under multiple stress conditions. PvAOX2;2_2 showed high induction under salt and heat stress, while PvAOX2;2_1 was significantly upregulated in response to cold stress. Collectively, these results suggest that AOX genes play important roles in the abiotic stress responses in common bean. This study provides valuable insights into the functional characteristics of AOX genes in leguminous crops and identifies potential candidate genes for the molecular improvement of stress tolerance in common bean.

Key words: common bean, AOX, leguminous crops, abiotic stress, expression pattern

闫知兰, 赵芹, 常甜达, 王一鸣, 王碧辉, 王鹏, 黄春国, 张会, 王利祥, 郝晓鹏, 赵波. 豆科作物AOX基因鉴定及其在普通菜豆响应非生物胁迫中的表达模式研究[J]. 作物学报, 2025, 51(7): 1769-1783.

YAN Zhi-Lan, ZHAO Qin, CHANG Tian-Da, WANG Yi-Ming, WANG Bi-Hui, WANG Peng, HUANG Chun-Guo, ZHANG Hui, WANG Li-Xiang, HAO Xiao-Peng, ZHAO Bo. Genome-wide identification and characterization of Alternative oxidase (AOX) genes in leguminous crops and their expression patterns in response to abiotic stresses in common bean[J]. Acta Agronomica Sinica, 2025, 51(7): 1769-1783.

图/表 14

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表1

表2

目标物种AOX基因家族蛋白质基本性质"

物种名称 Species name	基因名称 Gene ID	蛋白质长度 Protein length (aa)	相对分子质量 Molecular weight (Da)	等电点 pI	亲水性 GRAVY	不稳定性指数 Instability index	α-螺旋 Alpha helix (%)	延伸链 Extended strand (%)	β-折叠 Beta turn (%)	无规则卷曲 Random coil (%)	亚细胞定位 Subcellular localization
拟南芥Arabidopsis thaliana	AtAOX1D;1	318	36,202.41	8.65	−0.29	36.39	49.06	8.49	7.86	34.59	线粒体Mitochondrion
	AtAOX1B;3	325	37,432.24	8.55	−0.35	42.26	46.46	12.62	6.15	34.77	线粒体Mitochondrion
	AtAOX1A;3	354	39,979.87	8.56	−0.33	35.04	51.41	13.28	4.24	31.07	线粒体Mitochondrion
	AtAOX1C;3	329	37,816.51	6.91	−0.33	47.15	47.42	13.68	6.99	31.91	线粒体Mitochondrion
	AtAOX2;5	353	40,086.65	9.14	−0.17	29.53	43.20	15.41	5.44	35.95	线粒体Mitochondrion
大豆 Glycine max	GmAOX1A;4	321	36,476.17	8.57	−0.24	39.23	48.29	13.08	6.54	32.09	线粒体Mitochondrion
	GmAOX2;5	317	36,007.69	9.01	−0.18	35.81	55.84	9.15	7.26	27.76	线粒体Mitochondrion
	GmAOX2;8_1	326	37,115.48	8.68	−0.32	37.20	49.08	13.19	7.36	30.37	线粒体Mitochondrion
	GmAOX2;8_2	333	38,142.27	9.36	−0.27	38.75	51.95	11.41	8.41	28.23	线粒体Mitochondrion
普通菜豆 Phaseolus vulgaris	PvAOX1A;2	319	36,338.91	8.26	−0.30	40.34	55.17	9.09	5.02	30.72	线粒体Mitochondrion
	PvAOX2;2_2	329	37,772.83	9.04	−0.26	41.88	56.84	10.64	6.99	25.53	线粒体Mitochondrion
	PvAOX2;2_1	332	37,817.18	7.88	−0.38	36.44	53.61	9.94	4.82	31.63	线粒体Mitochondrion
绿豆 Vigna radiata	VrAOX2;9_1	332	37,952.48	8.67	−0.34	40.98	50.30	9.34	3.01	37.35	线粒体Mitochondrion
	VrAOX2;9_2	369	42,303.71	6.72	−0.27	41.53	46.07	13.55	6.50	33.88	线粒体Mitochondrion
	VrAOX1A;11	321	36,426.04	8.26	−0.28	37.00	47.35	10.59	5.61	36.45	线粒体Mitochondrion
宽叶菜豆Phaseolus acutifolius	PaAOX1A;2	319	36,369.90	8.22	−0.30	42.00	52.98	9.09	4.39	33.54	线粒体Mitochondrion
	PaAOX2;2_2	329	37,789.92	9.13	−0.23	41.09	48.02	11.55	6.99	33.43	线粒体Mitochondrion
	PaAOX2;2_1	332	37,802.21	8.36	−0.36	34.45	57.83	9.34	5.12	27.71	线粒体Mitochondrion

表2

图1

图2

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图3

附表2

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图4

附表4

图5

图6

图7

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物种名称 Species name	基因名称 Gene ID	登录号 Accession no.
拟南芥Arabidopsis thaliana	AtAOX1D;1	AT1G32350
	AtAOX1B;3	AT3G22360
	AtAOX1A;3	AT3G22370
	AtAOX1C;3	AT3G27620
	AtAOX2;5	AT5G64210
大豆Glycine max	GmAOX1A;4	GLYMA_04G123800
	GmAOX2;5	GLYMA_05G117200
	GmAOX2;8_1	GLYMA_08G072200
	GmAOX2;8_2	GLYMA_08G072300
普通菜豆Phaseolus vulgaris	PvAOX1A;2	PHAVU_002G127100g
	PvAOX2;2_2	PHAVU_002G209100g
	PvAOX2;2_1	PHAVU_002G209200g
绿豆Vigna radiata	VrAOX2;9_1	Vradi09g03140
	VrAOX2;9_2	Vradi09g03150
	VrAOX1A;11	Vradi11g08000
宽叶菜豆Phaseolus acutifolius	PaAOX1A;2	Phacu.CVR.002G149400
	PaAOX2;2_2	Phacu.CVR.002G238600
	PaAOX2;2_1	Phacu.CVR.002G238900
玉米Zea mays	ZmAOX4;2_1	Zm00001eb071880
	ZmAOX4;2_2	Zm00001eb071870
	ZmAOX5;2	Zm00001eb071890
	ZmAOX5;5	Zm00001eb251680
谷子Setaria italica	SiAOX4;VII_1	SETIT_010566mg
	SiAOX4;VII_2	SETIT_010539mg
	SiAOX5;VII_1	SETIT_010540mg
	SiAOX5;I	SETIT_017726mg
小麦Triticum aestivum	TaAOX3;3B	TraesCS3B02G087900
	TaAOX4;2B_1	TraesCS2B02G459000
	TaAOX4;2A_1	TraesCS2A02G438300
	TaAOX4;2A_2	TraesCS2A02G439100
	TaAOX4;2D_1	TraesCS2D02G436100
	TaAOX4;2B_2	TraesCS2B02G459100
	TaAOX4;2D_2	TraesCS2D02G43620
	TaAOX4;2A_3	TraesCS2A02G438200
	TaAOX5;2D	TraesCS2D02G436700
	TaAOX5;2B	TraesCS2B02G459300
	TaAOX5;2A	TraesCS2A02G439400
	TaAOX5;6D	TraesCS6D02G245800
	TaAOX5;6B	TraesCS6B02G296400
	TaAOX5;6A	TraesCS6A02G269100
高粱Sorghum bicolor	SbAOX4;6_1	SORBI_3006G202600
	SbAOX4;6_2	SORBI_3006G203000
	SbAOX5;6	SORBI_3006G202500
	SbAOX5;4	SORBI_3004G270500
水稻Oryza sativa	OsAOX3;2	Os02g0318100
	OsAOX4;4	Os04g0600300
	OsAOX5;4	Os04g0600200
	OSAOX5;2	Os02g0700400

基因名称Gene name	正向引物Forward primer (5'-3')	反向引物Reverse primer(5'-3')
PvAOX1A;2	TGACGTTCATGGAAGTGGCA	CCCTTAAAGTGGCGTCTGGT
PvAOX2;2_2	AGAGTGTGGTGGAGTCCAGT	ACATCCCTCCTACCATGCCA
PvAOX2;2_1	CACCTCCCAACAGCGAAGAT	ACAGTTCCATGGCCACTCAG
PvActin	GAAGTTCTCTTCCAACCATCC	TTTCCTTGCTCATTCTGTCCG

物种 Species	基因 ID Gene ID	转录本长度 Transcript length (bp)	染色体 Chr.	基因组位置 Genomic location	5'UTR数 Number of 5'UTR	3'UTR数 Number of 3'UTR	外显子数 Number of exon	内含子数 Number of intron
拟南芥 Arabidopsis thaliana	AtAOX1D;1	1429	1	11,666,886-11,668,690	1	1	4	3
	AtAOX1B;3	1229	3	7,904,097-7,905,576	1	1	4	3
	AtAOX1A;3	1764	3	7,906,521-7,908,746	1	1	4	3
	AtAOX1C;3	1346	3	10,229,045-10,230,707	1	1	4	3
	AtAOX2;5	1324	5	25,683,770-25,685,731	1	1	5	4
大豆 Glycine max	GmAOX1A;4	2448	4	16,009,828-16,014,505	1	1	4	3
	GmAOX2;5	954	5	31,012,789-31,015,519	0	0	5	3
	GmAOX2;8_1	1487	8	5,530,937-5,533,495	1	1	4	3
	GmAOX2;8_2	1527	8	5,534,625-5,537,952	1	1	4	3
普通菜豆 Phaseolus vulgaris	PvAOX1A;2	1353	2	25,631,296-25,635,132	1	1	4	3
	PvAOX2;2_2	1496	2	36,912,163-36,915,354	1	1	4	3
	PvAOX2;2_1	1263	2	36,916,649-36,918,323	1	1	4	3
绿豆 Vigna radiata	VrAOX2;9_1	1513	9	3,689,595-3,691,839	1	1	4	3
	VrAOX2;9_2	1133	9	3,719,512-3,724,510	1	0	6	5
	VrAOX1A;11	1282	11	8,412,330-8,414,861	1	1	4	3
宽叶菜豆Phaseolus acutifolius	PaAOX1A;2	1601	2	21,877,429-21,879,874	1	1	3	2
	PaAOX2;2_2	1024	2	32,731,956-32,734,686	0	1	4	3
	PaAOX2;2_1	1671	2	32,745,753-32,747,820	1	1	4	3

miRNA序号 miRNA accession	靶基因 ID Target accession	E值 Expectation	抑制作用 Inhibition	miRNA起始 miRNA start	miRNA终止 miRNA end	基因起始 Target start	基因终止 Target end
ath-miR863-3p	AtAOX1C;3	3.5	裂解Cleavage	1	21	1119	1139
ath-miR5021	AtAOX1C;3	2.5	裂解Cleavage	1	20	6	25
ath-miR414	GmAOX1A;4	2.5	裂解Cleavage	1	21	260	280
gra-miR8787	GmAOX1A;4	2.5	裂解Cleavage	1	23	2370	2392
osa-miR414	GmAOX1A;4	2.5	裂解Cleavage	1	21	260	280
mtr-miR2619b-5p	GmAOX1A;4	3.0	裂解Cleavage	1	21	2386	2406
aly-miR838-3p	PaAOX1A;2	2.5	裂解Cleavage	1	21	1493	1513
ptc-miR7814	PaAOX1A;2	2.5	裂解Cleavage	1	21	1244	1264
ata-miR1432-3p	PaAOX1A;2	3.0	裂解Cleavage	1	21	264	284
ath-miR414	PaAOX1A;2	3.0	裂解Cleavage	1	21	248	268
osa-miR414	PaAOX1A;2	3.0	裂解Cleavage	1	21	248	268
ppt-miR414	PaAOX1A;2	3.0	裂解Cleavage	1	21	248	268
ppt-miR1211-5p	PaAOX2;2_2	2.5	裂解Cleavage	1	21	1911	1931
gma-miR4392	PaAOX2;2_2	3.0	裂解Cleavage	1	22	715	736
sbi-miR6218-3p	PaAOX2;2_2	3.0	裂解Cleavage	1	21	2061	2081
ptc-miR6462c-5p	PaAOX2;2_1	3.0	裂解Cleavage	1	22	1513	1534
aly-miR838-3p	PvAOX1A;2	2.5	裂解Cleavage	1	21	657	677
ath-miR414	PvAOX1A;2	3.0	裂解Cleavage	1	21	119	139
osa-miR414	PvAOX1A;2	3.0	裂解Cleavage	1	21	119	139
-miR414	PvAOX1A;2	3.0	裂解Cleavage	1	21	119	139
aly-miR838-3p	VrAOX1A;11	3.0	裂解Cleavage	1	21	646	666
ath-miR1886.3	VrAOX1A;11	3.0	裂解Cleavage	1	21	1168	1188
sbi-miR5385	VrAOX1A;11	3.0	翻译Translation	1	22	172	193

豆科作物AOX基因鉴定及其在普通菜豆响应非生物胁迫中的表达模式研究

Genome-wide identification and characterization of Alternative oxidase (AOX) genes in leguminous crops and their expression patterns in response to abiotic stresses in common bean

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物种1 AOX AOXs in species1	染色体编号 Chr.	物种2 AOX AOXs in species2	染色体编号 Chr.	非同义替换率K_a	同义替换率 K_s	非同义替换/同义替换 K_a/K_s
AtAOX1D;1	1	AtAOX1B;3	3	0.29	2.04	0.14
AtAOX1D;1	1	AtAOX1C;3	3	0.29	1.64	0.18
AtAOX1B;3	3	AtAOX1A;3	3	0.13	1.04	0.13
AtAOX1B;3	3	AtAOX1C;3	3	0.09	0.57	0.15
AtAOX1B;3	3	AtAOX2;5	5	0.27	1.66	0.16
AtAOX1A;3	3	AtAOX1C;3	3	0.15	1.30	0.11
AtAOX1A;3	3	AtAOX2;5	5	0.32	2.67	0.12
AtAOX1C;3	3	AtAOX2;5	5	0.29	1.47	0.20
VrAOX2;9_1	9	VrAOX2;9_2	9	0.22	2.23	0.10
VrAOX2;9_1	9	PaAOX2;2_1	11	0.29	3.26	0.09
PaAOX2;2_1	11	AtAOX1D;1	1	0.26	3.53	0.07
VrAOX2;9_1	9	GmAOX2;5	5	0.22	1.53	0.14
VrAOX2;9_1	9	GmAOX2;8_1	8	0.04	0.50	0.08
PaAOX2;2_1	11	GmAOX1A;4	4	0.06	0.43	0.14
GmAOX1A;4	4	GmAOX2;8_1	8	0.31	3.26	0.10
GmAOX2;5	5	GmAOX2;8_1	8	0.24	1.54	0.15
GmAOX2;5	5	GmAOX2;8_2	8	0.04	0.18	0.19
GmAOX2;8_1	8	GmAOX2;8_2	8	0.23	1.39	0.16
GmAOX2;5	5	AtAOX2;5	5	0.27	2.42	0.11
GmAOX1A;4	4	PvAOX1A;2	2	0.05	0.37	0.13
GmAOX2;5	5	PvAOX2;2_2	2	0.06	0.29	0.20
GmAOX2;8_1	8	PvAOX2;2_2	2	0.20	1.47	0.14
PvAOX2;2_2	2	AtAOX2;5	5	0.25	3.41	0.07
PvAOX1A;2	2	PvAOX2;2_1	2	0.30	2.69	0.11
PvAOX1A;2	2	PaAOX2;2_1.1	11	0.09	0.57	0.15
PvAOX2;2_2	2	PvAOX2;2_1	2	0.23	1.53	0.15
PvAOX2;2_2	2	VrAOX2;9_1	9	0.22	1.59	0.14
PaAOX2;2_2	2	PaAOX2;2_1	2	0.23	1.55	0.15
PaAOX2;2_2	2	AtAOX2;5	5	0.24	2.80	0.09
PaAOX1A;2	2	GmAOX1A;4	4	0.04	0.36	0.12
PaAOX2;2_2	2	GmAOX2;5	5	0.05	0.29	0.18
PaAOX2;2_2	2	GmAOX2;8_1	8	0.20	1.58	0.13
PaAOX2;2_2	2	PvAOX2;2_2	2	0.01	0.03	0.45
PaAOX1A;2	2	PvAOX1A;2	2	0.01	0.08	0.13
PaAOX1A;2	2	PaAOX2;2_1	11	0.04	0.23	0.19
PaAOX2;2_2	2	VrAOX2;9_1	9	0.21	1.72	0.12

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