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Acta Agronomica Sinica ›› 2025, Vol. 51 ›› Issue (3): 650-666.doi: 10.3724/SP.J.1006.2025.44082

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

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 Online:2025-03-12 Published: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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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

Fig. 1

Schematic of vector constructions A: promoter vector; B: subcellular localization vector; C, D: overexpression vector; E: RNAi vector."

Table 1

Primers used in this study"

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

Fig. 2

GUS staining of IbHK5 gene promoter in transgenic Arabidopsis thaliana A: seedling; B: root; C: root tip; D: leaf; E: inflorescence. Scale bar: 5 mm."

Fig. 3

Subcellular localization of IbHK5"

Fig. 4

Relative expressions of IbHK5 in various transgenic Arabidopsis thaliana lines IbActin was used as the internal control, the L13 with lowest expression level was considered as ‘1’ with three biological replicates. *, ** indicate significant differences at the 0.05 and 0.01 probability levels according to Student’s t-test, respectively."

Fig. 5

Seeds germination rates and primary root lengths of IbHK5-OE transgenic Arabidopsis and WT on MS medium with mannitol or NaCl A-C: seed germination rates on MS medium without (control, A) or with 100 mmol L-1 mannitol (B) and 100 mmol L-1 NaCl (C), seed germination was calculated at the indicated times (1-7 d), respectively. D-I: primary root lengths of seedlings cultured for two weeks on MS medium without (D, E) or with 200 mmol L-1 mannitol (F, G) and 150 mmol L-1 NaCl (H, I), respectively. Each line contained five seedlings. J-K: seedlings etiolation (J) and primary root (K) on MS medium with 250 mmol L-1 NaCl. Seeds were germinated and grown for ten days on MS medium and then were transferred on MS medium with 250 mmol L-1 NaCl for five days. Each line contained 24 seedlings. Each treatment with three biological replicates. *, ** indicate significant differences at the 0.05 and 0.01 probability levels according to Student’s t-test, respectively."

Fig. 6

Responses of IbHK5-OE transgenic Arabidopsis and WT plants to drought and salt stress A: phenotypes of the transgenic plants vs. WT stressed by a four weeks drought period followed by three days of rewatering after two weeks of normal treatment. The six weeks normal treatment was used as the control. B: water loss rate of detached leaves from transgenic Arabidopsis and WT plants grown for four weeks under normal conditions. C: survival rate of transgenic and WT plants after three days of re-watering. D: phenotypes of the transgenic plants vs. WT stressed by a four weeks salt period after two weeks of normal treatment. The six weeks normal treatment was used as the control. E: total chlorophyll content. Each treatment with three biological replicates. *, ** indicate significant differences at the 0.05 and 0.01 probability levels according to Student’s t-test, respectively."

Fig. 7

ROS detection in IbHK5-OE transgenic Arabidopsis and WT plant leaves to drought and salt stress A: DAB staining. B: NBT staining. Scale bar in A and B: 5 mm. C: H2O2 content. D: MDA content. E-J: POD, SOD and CAT activities. Each treatment with three biological replicates. *, ** indicate significant differences at the 0.05 and 0.01 probability levels according to Student’s t-test, respectively."

Fig. 8

Transcript levels of ROS-scavenging system genes in the leaves of the IbHK5-OE transgenic and WT plants Biological replicates were performed three times per treatment. *, ** indicate significant differences at the 0.05 and 0.01 probability levels according to Student’s t-test, respectively."

Fig. 9

Protein-protein interactions between IbHK5 and Arabidopsis AHP1-AHP5"

Fig. 10

Pipeline of the A. rhizogenes-mediated in vivo root transgenic system in sweetpotato A: pTNRT vectors and A. rhizogenes bacterial colony; B: stem injection of A. rhizogenes bacterial with a syringe; C: cuttings cultured in the soil; D: 10 days after injection; E: 30 days after injection; F: 40 days after injection; G: 60 days after injection; H: transgenic hair roots with RFP fluorescence signals; I: non-transgenic roots without RFP fluorescence signals. Scale bar: 1 cm."

Fig. 11

Screening and identification of positive transgenic sweetpotato plants Transgenic hair roots with RFP fluorescence signals 60 days after stem injection of A. rhizogenes bacterial in IbHK5-OE (A), IbHK5-RNAi (B) and vector control (C) sweetpotato plants, wild type plants without fluorescence signals in roots used as control (D). E: identification of positive transgenic hair roots with PCR, among which four representative lines were selected for each vector, NC, negative control. F: relative expressions of IbHK5 in transgenic hair roots. Scale bars: 1 cm. *, ** indicate significant differences at the 0.05 and 0.01 probability levels according to Student’s t-test, respectively."

Fig. 12

Phenotypes and antioxidant enzyme activities of IbHK5-OE, IbHK5-RNAi, and vector control (VC) sweetpotato seedlings with drought and salt treatment A: growth of seedlings with drought and salt treatment. B: fresh root weight. C: POD activity. D: SOD activity. E: CAT activity. F: H2O2 content. G: MDA content. Each treatment contained 10 plants with three biological replicates. Scale bars: 5 cm. *, ** indicate significant differences at the 0.05 and 0.01 probability levels according to Student’s t-test, respectively."

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