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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. 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,*()   

  1. 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:

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

附表1

10种作物AOX基因登录号"

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

表1

实时荧光定量PCR引物序列表"

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

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

图1

4种豆科作物及拟南芥AOX蛋白的三维结构 图中目标物种中的AOX蛋白按照亲缘关系分为3个亚组, 分别为Subgroup I、Subgroup II和Subgroup III, 蛋白三维结构下面为每个AOX蛋白的名称。"

图2

10个物种AOX家族成员系统发育树及4种豆科作物与拟南芥AOX成员之间的共线性分析 A: 10个物种AOX家族成员的系统发育进化树。各分支节点上的数字代表自展值, 自展值数值越大, 代表这一分支可信度更高。B: 5个物种AOX成员之间共线性图。背景中的灰色线表示不同植物基因组中的所有的共线关系, 而彩色线则表示不同物种AOX成员间的共线性。At: 拟南芥; Os: 水稻; Gm: 大豆; Ta: 小麦; Pa: 宽叶菜豆; Pv: 普通菜豆; Vr: 绿豆; Si: 谷子; Zm: 玉米; Sb: 高粱。"

附图1

目标物种中AOX基因的染色体定位 A: 拟南芥; B: 宽叶菜豆; C: 绿豆; D: 普通菜豆; E: 大豆。"

图3

5个物种AOX基因家族成员的系统发育树(A)、保守基序(B)、保守结构域(C)和基因结构图(D)"

附表2

目标物种中AOX基因家族成员基本理化性质"

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

附表3

不同物种之间直系同源AOX蛋白的Ka/Ks"

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Ka 同义替换率
Ks
非同义替换/同义替换
Ka/Ks
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

图4

目标物种中AOX基因启动子区域顺式作用元件分析 图中AOX中预测的顺式作用元件位于起始密码子的上游2000 bp的启动子区域。AOX基因的顺式作用元件共分为3类, 从左到右依次为与植物生长、激素响应以及非生物和生物胁迫响应相关的元件。热图每个方框中的数字表示对应的顺式调控元件的数量, 右侧的柱形图展示各个基因中各类顺式调控元件的统计结果。"

附表4

psRNATarget在线工具鉴定靶向作用AOX基因的假定miRNA"

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

图5

普通菜豆AOX基因在不同生育期的不同组织转录表达水平分析 普通菜豆AOX基因在不同组织的表达水平热图, 数据从Phytozome数据库通过关键词搜索得到。热图颜色代表基因转录本水平的高低, 蓝色表示低值, 红色表示高值; 色阶变化表示表达量的高低, 转录本数据进行log归一化、基因所在列进行正态标准化0-1标准化, 热图中数值表示原始的FPKM数值。"

图6

普通菜豆AOX基因在碱胁迫(A)、盐胁迫(B)和PEG干旱胁迫(C)下的相对表达量 *、**、***和****分别表示在0.05、0.01、0.001和0.0001水平差异显著。ns表示差异不显著。AS、SA和PEG分别代表碱胁迫、盐胁迫和PEG胁迫的处理组, CK代表相应的对照组, 后面数字为处理时长。"

图7

普通菜豆AOX基因在冷胁迫(A)和高温胁迫(B)下的相对表达量 *、**、***和****分别表示在0.05、0.01、0.001和0.0001水平差异显著。ns表示差异不显著。CS和HT分别代表冷胁迫和高温胁迫的处理组, CK代表相应的对照组, 后面数字为处理时长。"

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