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作物学报 ›› 2025, Vol. 51 ›› Issue (3): 650-666.doi: 10.3724/SP.J.1006.2025.44082

• 作物遗传育种·种质资源·分子遗传学 • 上一篇    下一篇

甘薯组氨酸激酶蛋白IbHK5响应干旱和盐胁迫的功能分析

霍如雪1,2(), 葛祥菡1, 石嘉1, 李雪蕊1, 戴圣杰1, 刘振宁1,*(), 李宗芸2,*()   

  1. 1临沂大学农林科学学院, 山东临沂 276000
    2江苏师范大学生命科学学院, 江苏徐州 221116
  • 收稿日期:2024-05-15 接受日期:2024-12-12 出版日期:2025-03-12 网络出版日期:2024-12-12
  • 通讯作者: *刘振宁, E-mail: liuzhenning@lyu.edu.cn; 李宗芸, E-mail: zongyunli@jsnu.edu.cn
  • 作者简介:E-mail: huoruxue@lyu.edu.cn
  • 基金资助:
    财政部和农业农村部国家现代农业产业技术体系建设专项(CARS-10);江苏省高校生物学优势学科建设项目(PAPD);国家自然科学基金项目(32070344);山东省高等学校青创科技计划项目(2021KJ055)

Functional analysis of the sweetpotato histidine kinase protein IbHK5 in response to drought and salt stresses

HUO Ru-Xue1,2(), GE Xiang-Han1, SHI Jia1, LI Xue-Rui1, DAI Sheng-Jie1, LIU Zhen-Ning1,*(), LI Zong-Yun2,*()   

  1. 1College of Agriculture and Forestry Sciences, Linyi University, Linyi 276000, Shandong, China
    2School of Life Sciences, Jiangsu Normal University, Xuzhou 221116, Jiangsu, China
  • Received:2024-05-15 Accepted:2024-12-12 Published:2025-03-12 Published online:2024-12-12
  • Contact: *E-mail: liuzhenning@lyu.edu.cn; E-mail: zongyunli@jsnu.edu.cn
  • Supported by:
    China Agriculture Research System of MOF and MARA(CARS-10);Priority Academic Program Development of Jiangsu Higher Education Institutions(PAPD);National Natural Science Foundation of China(32070344);Innovation Team of Youth Technology Project of High School in Shandong Province(2021KJ055)

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摘要：

组氨酸激酶是植物双组分信号系统中的一类重要元件, 参与了植物生长发育、逆境响应等多种生物学功能。本研究在甘薯中鉴定到一个与拟南芥AHK5同源的基因IbHK5。亚细胞定位研究表明, IbHK5蛋白主要定位于细胞质和细胞核中。利用拟南芥异源超表达和甘薯发状根遗传转化技术研究了IbHK5参与干旱胁迫和盐胁迫的生物学功能。结果表明, IbHK5在拟南芥中的异源超表达能够增强拟南芥的耐旱性和耐盐性, 超表达株系中表现出较高的POD、SOD和CAT酶活, 较少的H2O2和O2-的积累, 以及相对表达量较高的POD、SOD、CAT和GPX等ROS清除系统相关基因。同样, IbHK5在甘薯中的超表达也能增强甘薯的耐旱性和耐盐性, 甘薯发状根也表现出较高的POD、SOD和CAT酶活, 较少的H2O2和O2-的积累。酵母双杂交试验表明, IbHK5能与拟南芥AHP1、AHP2、AHP3和AHP5蛋白互作。上述结果证实IbHK5是参与干旱胁迫和盐胁迫的一个正调控因子。研究结果有助于解析甘薯抵御干旱胁迫和盐胁迫的生理机制与分子机制, 也能够为耐干旱、耐盐的甘薯定向改良和品种选育提供一定的理论依据。

关键词: 甘薯, 双组分信号系统, 组氨酸激酶, IbHK5, 干旱胁迫, 盐胁迫

Abstract:

Histidine kinase is a key component of the two-component system in plants, playing a crucial role in regulating plant growth, development, and responses to various stresses. In this study, IbHK5, a histidine kinase homologous to Arabidopsis AHK5, was identified in sweetpotato. Subcellular localization analysis revealed that the IbHK5 protein is localized in both the cytoplasm and nucleus. To investigate its biological function in response to drought and salt stress, IbHK5was ectopically expressed in Arabidopsis and overexpressed in sweetpotato using an Agrobacterium rhizogenes-mediated in vivo root transformation system. The results showed that overexpression of IbHK5 in Arabidopsis enhanced both drought and salt tolerance. The transgenic plants exhibited higher activities of POD, SOD, and CAT enzymes, lower levels of H2O2 and MDA, and increased expression of stress-related genes, including AtPOD, AtSOD, AtCAT, and AtGPX. Similarly, overexpression of IbHK5 in sweetpotato enhanced drought and salt tolerance, with transgenic hairy roots showing elevated POD, SOD, and CAT enzyme activities as well as reduced H2O2 and MDA content. Furthermore, yeast two-hybrid assays demonstrated that IbHK5 interacts with Arabidopsis proteins AHP1, AHP2, AHP3, and AHP5, indicating its involvement in signal transduction pathways. These results suggest that IbHK5 is a positive regulator of drought and salt stress tolerance. This study provides insights into the physiological and molecular mechanisms underlying drought and salt stress responses in sweetpotato and offers a theoretical foundation for the genetic improvement and breeding of drought- and salt-tolerant sweetpotato varieties.

Key words: sweetpotato, two component system, histidine kinase, IbHK5, drought stress, salt stress

图1

载体构建示意图 A: 启动子表达载体; B: 亚细胞定位载体; C和D: 超表达载体; E: RNAi载体。"

表1

本研究中使用的引物"

引物名称
Primer name		 引物序列
Primer sequence (5′-3′)		 用途
Usage
IbHK5pro-F GGGGTACCAACCTCTATCGAAGAACCACGGAGA IbHK5启动子序列克隆
Clone of IbHK5 promoter sequence
IbHK5pro-R CGGGATCCCTTCGAGTACCACTATATTGCATGC
1300-F CTGGAAAGCGGGCAGTGAG 启动子表达株系鉴定
Identification of promoter reporter lines
IbHK5pro-Seq-R AGGTGGCATTTTTCCCTCTCTTTCT
IbHK5CDS-F GGGGTACCATGGTATCTGAGATGGAGAATGCTC 亚细胞定位载体构建
Construction of subcellular localization vector
IbHK5CDS-R1 GCTCTAGACAGGCGATGGCGCTGCGGCAAA
IbHK5CDS-F GGGGTACCATGGTATCTGAGATGGAGAATGCTC 拟南芥超表达载体构建
Construction of Arabidopsis overexpression vector
IbHK5CDS-R2 GCTCTAGATTACAGGCGATGGCGCTGCGGCAAA
IbHK5CDS-Seq-F TGTGAATAATGGAATAGAAGCTGTG 拟南芥超表达株系鉴定
Identification of Arabidopsis overexpression lines
NOST-R CCCAAGCTTATCGAATTCGATCTAGTAACATAGA
IbHK5CDS(TNRT)-F GTTCTTCACTGTTGATACACGCGTATGGTATCTGAGATGGAGAATGCTC 甘薯超表达载体构建
Construction of sweetpotato overexpression vector
IbHK5CDS(TNRT)-R AGTTGTTGATTCAGAATTGTCGACTTACAGGCGATGGCGCTGCGGCAAA
IbHK59CDS-Seq-F TGTGAATAATGGAATAGAAGCTGTG 甘薯超表达株系鉴定
Identification of sweetpotato overexpression lines
HSPT-R CAAGCCAAGAAAAAAACACAAACT
IbHK5-T1-F ACTAGGGTCTCGCACCAGACGATGCAAATTCTGGCTTCTTCCA RNAi载体构建
Construction of RNAi vector
IbHK5-T1-R ACTAGGGTCTCTGCAGGAATGTGAGCTTTGCCTGAAAGAACTTTCG
IbHK5-T2-F ACTAGGGTCTCGGCTTGAATGTGAGCTTTGCCTGAAAGAACTTTCG
IbHK5-T2-R ACTAGGGTCTCTACCGAGACGATGCAAATTCTGGCTTCTTCCA
35S-F CACGGGGGACTCTTGCCACC 甘薯RNAi株系鉴定
Identification of sweetpotato RNAi lines
Linker(c-)-R AAGCTTCTGTAACTATCATCATCA
IbHK5-qRT-F GAAACCGAACTTAACAGAACAATC qRT-PCR分析
qRT-PCR analysis
IbHK5-qRT-R CAAATCACCCGAAGACAACAT
AtActin7-qRT-F GGAACTGGAATGGTGAAGGCTG qRT-PCR分析
qRT-PCR analysis
AtActin7-qRT-R CGATTGGATACTTCAGAGTGAGGA
IbActin-qRT-F CTGGTGTTATGGTTGGGATGG
IbActin-qRT-R GGGGTGCCTCGGTAAGAAG
AtSOD-qRT-F ATGAGAAGTTCTATGAAGAG
AtSOD-qRT-R GTCTTTATGTAATCTGGT
AtPOD-qRT-F TCCGGGAGCACACCATTGG
AtPOD-qRT-R TGGTCGGAATTCAACAG
AtCAT-qRT-F GCAACTACCCCCGAGTGGAAA
AtCAT-qRT-R TGTTCAGAACCAAGCGACCA
AtGPX-qRT-F ATGGCGACGAAGGAACCAG
AtGPX-qRT-R ATCGCCGAAGATTCCCCATTT
AHP1-pGBKT7-F TGGCCATGGAGGCCGAATTCATGGATTTGGTTCAGAAGCAGAAG 酵母双杂交
Yeast two hybrid
AHP1-pGBKT7-R CGCTGCAGGTCGACGGATCCTCAAAATCCGAGTTCGACGGCCGG
AHP2-pGBKT7-F TGGCCATGGAGGCCGAATTCATGGACGCTCTCATTGCTCAGCTT
AHP2-pGBKT7-R CGCTGCAGGTCGACGGATCCTTAGTTAATATCCACTTGAGGAAC
AHP3-pGBKT7-F TGGCCATGGAGGCCGAATTCATGGACACACTCATTGCTCAGTTA
AHP3-pGBKT7-R CGCTGCAGGTCGACGGATCCTTATATATCCACTTGAGGGATTCT
AHP4-pGBKT7-F TGGCCATGGAGGCCGAATTCATGCAGAGGCAAGTGGCACTCATC
AHP4-pGBKT7-R CGCTGCAGGTCGACGGATCCTTACTTGGGCCTACGTGCTGTCTC
AHP5-pGBKT7-F TGGCCATGGAGGCCGAATTCATGAACACCATCGTCGTTGCTCAG
AHP5-pGBKT7-R CGCTGCAGGTCGACGGATCCCTAATTTATATCCACTTGAGGAAT
IbHK5-pGADT7-F CCATGGAGGCCAGTGAATTCATGGTATCTGAGATGGAGAATG
IbHK5-pGADT7-R AGCTCGAGCTCGATGGATCCTTACAGGCGATGGCGCTGCGGC

图2

转基因拟南芥中IbHK5基因启动子的GUS染色 A: 幼苗; B: 主根; C: 根尖; D: 叶片; E: 花序。标尺为5 mm。"

图3

IbHK5蛋白的亚细胞定位"

图4

拟南芥转基因株系中IbHK5基因的相对表达量 以IbActin为内参基因, 表达量最低的株系L13的相对表达水平作为“1”, 3次生物学重复。经Student’s t检验, *、**分别表示在0.05和0.01水平上差异显著。"

图5

IbHK5超表达株系和WT在添加mannitol或NaCl的MS培养基上种子的发芽率和主根长 A~C为添加0 (A)、100 mmol L-1 mannitol (B)和100 mmol L-1 NaCl (C)的MS培养基上种子的发芽率, 在第1天到第7天每天统计一次发芽率。D~I为添加0 (D、E)、200 mmol L-1 mannitol (F、G)和150 mmol L-1 NaCl (H、I)的MS培养基上生长2周后的主根长度, 每个株系5棵幼苗。J~K为添加250 mmol L-1 NaCl的MS培养基上幼苗黄化情况(J)和主根长度(K)。种子播于MS培养基上生长10 d后再将幼苗移至添加250 mmol L-1 NaCl的MS培养基上生长5 d, 每个株系24棵幼苗。每个处理3次生物学重复。经Student’s t检验, *、**分别表示在0.05和0.01水平上差异显著。"

图6

IbHK5超表达株系和WT对干旱和盐胁迫的响应 A: 超表达株系和WT幼苗先正常培养2周, 然后干旱胁迫处理4周以及复水3 d后的表型, 以幼苗正常培养6周作为对照。B: 超表达株系和WT幼苗正常培养4周后离体叶片的失水率。C: 超表达株系和WT复水3 d后的存活率。D: 超表达株系和WT幼苗先正常培养2周, 然后盐胁迫处理4周后的表型, 以幼苗正常培养6周作为对照。E: 总叶绿素含量。每个处理3次生物学重复。经Student’s t检验, *、**分别表示在0.05和0.01水平上差异显著。"

图7

IbHK5超表达株系和WT在干旱和盐胁迫处理下叶片中ROS的检测 A: DAB染色。B: NBT染色。A和B标尺为5 mm。C: H2O2含量。D: MDA含量。E~J: POD、SOD和CAT的酶活性。每个处理3次生物学重复。经Student’s t检验, *、**分别表示在0.05和0.01水平上差异显著。"

图8

IbHK5超表达株系和WT在干旱胁迫、盐胁迫处理条件下叶片中ROS清除系统相关基因的表达 每个处理3次生物学重复。经Student’s t检验, *、**分别表示在0.05和0.01水平上差异显著。"

图9

IbHK5与拟南芥AHP1~AHP5的蛋白互作情况"

图10

发根农杆菌介导的甘薯遗传转化体系流程图 A: 载体构建和发根农杆菌菌板; B: 茎部注射; C: 注射后的茎段插入培养土中培养; D: 注射10 d后的茎段; E: 注射30 d后的茎段; F: 注射40 d后的茎段; G: 注射60 d后的茎段; H: 带有红色荧光蛋白信号的发状转化根; I: 无红色荧光蛋白信号的非转化根。标尺为1 cm。"

图11

甘薯阳性转基因根系的筛选与鉴定 IbHK5-OE (A)、IbHK5-RNAi (B)和VC (C)甘薯发状根中的红色荧光信号, 根系中无荧光信号的野生型植株WT为对照(D)。E: 甘薯阳性转基因发状根的PCR鉴定, 每个载体均选取其中4个代表性根系, NC表示阴性对照。F: IbHK5在甘薯发状根中的相对表达量。标尺为1 cm。经Student’s t检验, *、**分别表示在0.05和0.01水平上差异显著。"

图12

IbHK5-OE、IbHK5-RNAi和VC空载植株的甘薯幼苗经干旱和盐胁迫处理后的表型和酶活性测定 A: 甘薯幼苗经干旱和盐胁迫处理后的生长情况。B: 根的鲜重。C: POD酶活性。D: SOD酶活性。E: CAT酶活性。F: H2O2含量。G: MDA含量。每个处理10株, 3次生物学重复。标尺为5 cm。经Student’s t检验, *、**分别表示在0.05和0.01水平上差异显著。"

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