Wheat methionine sulfoxide reductase A4.1 interacts with heme oxygenase 1 to enhance seedling tolerance to salinity or drought stress

  • Pengcheng Ding
  • Linlin Fang
  • Guangling Wang
  • Xiang Li
  • Shu Huang
  • Yankun Gao
  • Jiantang Zhu
  • Langtao Xiao
  • Jianhua Tong
  • Fanguo ChenEmail author
  • Guangmin Xia

Key message

Here, a functional characterization of a wheat MSR has been presented: this protein makes a contribution to the plant’s tolerance of abiotic stress, acting through its catalytic capacity and its modulation of ROS and ABA pathways.


The molecular mechanism and function of certain members of the methionine sulfoxide reductase (MSR) gene family have been defined, however, these analyses have not included the wheat equivalents. The wheat MSR gene TaMSRA4.1 is inducible by salinity and drought stress and in this study, we demonstrate that its activity is restricted to the Met-S-SO enantiomer, and its subcellular localization is in the chloroplast. Furthermore, constitutive expression of TaMSRA4.1 enhanced the salinity and drought tolerance of wheat and Arabidopsis thaliana. In these plants constitutively expressing TaMSRA4.1, the accumulation of reactive oxygen species (ROS) was found to be influenced through the modulation of genes encoding proteins involved in ROS signaling, generation and scavenging, while the level of endogenous abscisic acid (ABA), and the sensitivity of stomatal guard cells to exogenous ABA, was increased. A yeast two-hybrid screen, bimolecular fluorescence complementation and co-immunoprecipitation assays demonstrated that heme oxygenase 1 (HO1) interacted with TaMSRA4.1, and that this interaction depended on a TaHO1 C-terminal domain. In plants subjected to salinity or drought stress, TaMSRA4.1 reversed the oxidation of TaHO1, activating ROS and ABA signaling pathways, but not in the absence of HO1. The aforementioned properties advocate TaMSRA4.1 as a candidate for plant genetic enhancement.


Triticum aestivum Methionine sulfoxide reductase A4.1 Heme oxygenase 1 Salinity stress Drought stress Abscisic acid Reactive oxygen species 



Methionine sulfoxide reductase


Methionine sulfoxide


Heme oxygenase 1


Zinc protoporphyrin IX


Yeast two-hybrid


Bimolecular fluorescence complementation




Reactive oxygen species



We thank Mingyi Bai (Shandong University, Jinan, China) for providing the MPH and YFPC/YFPN vectors. This research was supported by the Natural Science Foundation of China (31471486, 31271706, 31570372) and an Agricultural Industrialization Development Project of high-quality seed from Shandong Province (2013).

Author contributions

FC designed the research. FC and PD wrote the manuscript. PD, LF, GW, SH, XL, YG, JZ, LX, and JT performed the experiments. FC, PD, and GX contributed to data analysis. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11103_2019_901_MOESM1_ESM.tif (5 mb)
Supplementary material 1 (TIFF 5078 kb) Figure S1 Potential interactor of MSRA4 according to the STRING database. (a) Setaria italica MSRA4, accession number: XM_004983571; (b) Brachypodium distachyon MSRA4, accession number: XM_014901147; (c) Sorghum bicolor MSRA4, accession number: XM_002467431; (d) Oryza sativa japonica MSRA4, accession number: XM_015758657; (e) Zea mays MSRA4, accession number: KP168441.1; (f) Glycine max MSRA4: accession number: XM_006595530. TaHO1 homologs are indicated with red boxes
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Supplementary material 2 (TIFF 4073 kb) Figure S2 The transcriptional response of TaMSRA4.1 in three-leaf-stage wheat seedling exposed to (a) 10 mM H2O2 and (b) 100 μM ABA. (c) The predicted structure of TaMSRA4.1, including its C-terminal PMSR domain. The numbers represent the order of amino acids of TaMSRA4.1. (d) The subcellular localization of TaHO1 in Arabidopsis protoplast. GFP: control transgene (p35S::GFP). Scale bar: 10 μm
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Supplementary material 3 (TIFF 15224 kb) Figure S3 The induced expression and purification of recombinant wheat proteins. Western blot images of (a) E. coli expressing TaMSRA4.1 (the purified protein is shown in the right-hand panel); and (b) E. coli expressing TaHO1 (the purified protein is shown in the right-hand panel). M: molecular weight marker
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Supplementary material 4 (TIFF 2225 kb) Figure S4 The expression pattern of TaMSRA4.1 in cv. SR3 and YM20 under salt and drought stress, and authentication of the TaMSRA4.1 transgene in wheat and A. thaliana. The transcriptional response of TaMSRA4.1 in cv. SR3 or YM20 exposed to (a) 100 mM NaCl and (b) 10% PEG. (c) PCR-based detection of T2 transgenic plants. RT-qPCR analysis showing that TaMSRA4.1 was transcribed in (d) wheat and (e) A. thaliana. The wheat Actin gene (AB181991) and AtActin (At3g18780) were the respective reference sequences. Data are presented as the mean ± SE (n = 3). *P < 0.05, **P < 0.01 by Student’s t-test. (f) Schematic diagram of the structure of AtMSRA4 and the T-DNA insertion site of the mutant. ATG and TAA indicate the start and stop codons, respectively. (g) PCR-based confirmation of the T-DNA insertion site in the msra4 mutant. Amplicons generated from the following primer pairs (Table S1): Lanes 1,4: LP/RP; lanes 2,5: LP/LBb1.3; and lanes 3,6: RP/LBb1.3. M: molecular weight marker. (h) Transcription profile of AtMSRA4 in Col-0 and the msra4 mutant, as detected by RT-PCR with AtActin as the reference sequence
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Supplementary material 5 (TIFF 16998 kb) Figure S5 The ROS level in transgenic wheat plants following NaCl or PEG treatment, and the appearance of transgenic A. thaliana plants exposed to salt or drought conditions. ROS level in the leaves of 1-week-old wheat seedlings raised under (a, f) non-stressed conditions, (b, g) 100 mM NaCl and (c, h) 10% PEG. Tissue stained with (a-c) NBT and (f–h) DAB. (d) H2O2 content of seedlings exposed to stress. (e) CAT activity, FW: fresh weight. (i, j) The performance of Col-0, transgenic and mutant A. thaliana seedlings under normal and (i) salinity or (j) drought stress conditions. (k) Survival rate following exposure to drought or salinity. In the latter treatment, plants with > 50% green were classed as survivors; in the former, plants able to recover growth after removal of the stressor were considered as survivors. Each experimental unit was composed of 20 plants. Data are presented as the mean ± SE (n = 3). *P < 0.05, **P < 0.01 by Student’s t-test. (l) Water loss rates from detached leaves of Col-0, transgenic and mutant A. thaliana plants. Leaves at similar developmental stages were excised and weighed at the indicated time after detachment. The proportion of fresh weight loss was calculated on the basis of the initial weight of the leaves. Each data point represents the mean with SE (n = 30)
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Supplementary material 6 (TIFF 15691 kb) Figure S6 The phenotype of transgenic A. thaliana under H2O2 treatment, and ROS levels in transgenic A. thaliana exposed to salinity or drought stress. The appearance of seedlings of Col-0, AtOE1 and AtOE2 lines and the msra4 mutant grown (a) under non-stressed conditions and (b) in the presence of 1 mM H2O2. The leaves of seedlings of Col-0, AtOE1 and AtOE2 lines and the msra4 mutant grown (c) under non-stressed conditions, (d) in the presence of 100 mM NaCl or (e) 16% PEG, stained by DAB (upper panel) or NBT (lower panel). (f) The root lengths of the seedlings grown under non-stressed conditions or in the presence of 1 mM or 1.5 mM H2O2 for 14 days. (g) The H2O2 content, (h) CAT activity, (i) SOD activity and (j) MDA content of seedlings grown under non-stressed conditions or in the presence of 100 mM NaCl or 16% PEG. FW: fresh weight. Data are presented as the mean ± SE (n = 3). *P < 0.05, **P < 0.01 by Student’s t-test
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Supplementary material 7 (TIFF 3836 kb) Figure S7 The expression patterns of certain ROS-associated genes in Col-0, AtOE line and msra4 mutant plants exposed to 200 mM NaCl or 16% PEG. (a, d) ROS signaling genes, (b, e) ROS generation genes and (c, f) ROS scavenging genes. Transcript levels determined by qRT-PCR, using AtActin as the reference. Data are presented as the mean ± SE (n = 3). ANAC047: A. thaliana NAC transcription factor 047; OXI1: oxidative signal-inducible1; MAPK11: mitogen-activated protein kinase 11; DREB2A: dehydration responsive element binding protein 2A; WRKY40: WRKY DNA-binding protein 40; RbohC/D/E/F/G/I: respiratory burst oxidase homolog C/D/E/F/G/I; CAT1/2/3: catalase 1/2/3; FeSOD1/2/3: iron superoxide dismutase; Cu/ZnSOD1/2: copper/zinc superoxide dismutase. (g) The relative transcriptional level of three NADPH oxidative genes in wheat. (h) The relative transcriptional level of two oxidoreductase genes in wheat. Data are presented as the mean ± SE (n = 3), *P < 0.05, **P < 0.01 by Student’s t-test
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Supplementary material 8 (TIFF 417 kb) Figure S8 The expression patterns of certain marker genes of the ABA signaling pathway in Col-0, AtOE line and msra4 mutant plants. Transcript levels in 4-week-old seedlings of genes involved in (a) the ABA-dependent stress response pathway and (b) the ABA synthesis pathway. Data are presented as the mean ± SE (n = 3), *P < 0.05, **P < 0.01 by Student’s t-test
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Supplementary material 9 (TIFF 4850 kb) Figure S9 The tertiary structure of TaHO1 and the location of its surface-exposed Met residues. (a) The tertiary structure of TaHO1. The α-helix is displayed in red, the loop in blue, and the Met residues in green. (b) The surface-displayed tertiary structure of TaHO1. Met residues are displayed in red
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Supplementary material 10 (TIFF 23379 kb) Figure S10 ROS levels in the leaves of YM20 and TaOE lines under control and salt or drought stress conditions in the presence of ZnPP, and in the leaves of Col-0, hy1-100 and TaMSRA4.1/hy1-100 lines under control conditions. ROS levels in the leaves of 1-week-old wheat seedlings raised under (a, c) non-stressed conditions, (b, d) 100 mM NaCl and (e, f) 10% PEG. Tissue stained with (a, b, e) NBT or (c, d, f) DAB. (g) ROS levels in the leaves of 4-week-old A. thaliana seedlings raised under non-stress conditions. Tissue stained with DAB (upper panel) or NBT (lower panel). Phenotype of Col-0, msra4 mutant and TaHO1/msra4 plants grown under (h) no stress, (i) 100 mM NaCl and (j) 200 mM mannitol. (k) Root lengths of the seedlings from (h-j)
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Supplementary material 11 (TIFF 10416 kb) Figure S11 The expression pattern of TaHO1 in cv. SR3 and YM20 under salt, drought or ABA stresses and the controls of the BiFC assay used to identify the TaMSRA4.1-TaHO1 and TaMSRA4.1-AtHO1 interaction. The transcriptional response of TaHO1 in cv. SR3 or YM20 exposed to (a) 100 mM NaCl and (b) 10% PEG. (c) The expression pattern of TaHO1 in SR3 exposed to 200 μM ABA. (d) The HO enzyme activity of wheat seedlings under control and salt or drought conditions. (e) The HO enzyme activity in A. thaliana plants constitutively expressing TaMSRA4.1 and in the msra4 mutant. (f) The HO enzyme activity of the A. thaliana seedlings under control and salt or drought conditions. Data are presented as the mean ± SE (n = 3). *P < 0.05, **P < 0.01 by Student’s t-test. (g) The controls of the BiFC assay used to identify the TaMSRA4.1-TaHO1 and TaMSRA4.1-AtHO1 interaction. Scale bar: 20 μm
11103_2019_901_MOESM12_ESM.tif (8.2 mb)
Supplementary material 12 (TIFF 8376 kb) Figure S12 Phenotype of Col-0, hy1-100 mutant and TaMSRA4.1/hy1-100 plants grown under (a) no stress, (b) 1 mM H2O2 and (c) 5 μM ABA. (d) Root lengths of the seedlings from (a-c). Transcript levels in 4-week-old Col-0, hy1-100 and TaMSRA4.1/hy1-100 seedlings of genes involved in (e, f) the ABA synthesis pathway and (g, h) the ABA-dependent stress response pathway. Transcript levels in 4-week-old Col-0 and hy1-100 seedlings of genes involved in (i-l) ROS generation and (m-p) ROS scavenging. One-week-old seedlings were exposed to 1 mM H2O2 or 5 μM ABA for 2 weeks. Data are presented as the mean ± SE (n = 3), *P < 0.05, **P < 0.01 by Student’s t-test
11103_2019_901_MOESM13_ESM.tif (17.2 mb)
Supplementary material 13 (TIFF 17589 kb) Figure S13 The appearance of AtOE and msra4 lines compared to that of Col-0 raised in the presence of 1.5 g/L Hb or 10 μM hematin with and without stress. The appearance of the Col-0, AtOE line and msra4 plants grown in a medium containing 1.5 g/L Hb (a) under non-stressed conditions, and in the presence of (b) 100 mM NaCl and (c) 200 mM mannitol. (d) Root lengths of the seedlings from (a-c). The appearance of the Col-0, AtOE line and msra4 plants grown in a medium containing 10 μM hematin (e) under non-stressed conditions, and in the presence of (f) 100 mM NaCl and (g) 200 mM mannitol. (h) Root lengths of the seedlings from (e–g). One-week-old seedlings were exposed to 100 mM NaCl or 200 mM mannitol with 1.5 g/L Hb or 10 μM hematin for two weeks. Data are presented as the mean ± SE (n = 3), *P < 0.05, **P < 0.01 by Student’s t-test
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Supplementary material 14 (TIFF 44 kb) Figure S14 A working model of TaMSRA4.1 in wheat. Abiotic stress induces the expression of TaMSRA4.1, which reverses the oxidation of TaHO1. TaHO1 modulates ABA synthesis/ABA signaling pathways and redox homeostasis, both of which induce stomatal closure, accounting for salinity and drought tolerance. Arrowed lines indicate a promotion effect
11103_2019_901_MOESM15_ESM.pdf (103 kb)
Supplementary material 15 (PDF 103 kb)
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Supplementary material 16 (DOCX 21 kb) Methods S1 Methods used for sub-cellular localization, yeast two hybrid experiments, bimolecular fluorescence complementation (BiFC) assays and co-immunoprecipitation (Co-IP) assays


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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Pengcheng Ding
    • 1
  • Linlin Fang
    • 1
  • Guangling Wang
    • 1
  • Xiang Li
    • 1
  • Shu Huang
    • 1
  • Yankun Gao
    • 1
  • Jiantang Zhu
    • 1
  • Langtao Xiao
    • 2
  • Jianhua Tong
    • 2
  • Fanguo Chen
    • 1
    Email author
  • Guangmin Xia
    • 1
  1. 1.The Key Laboratory of Plant Development and Environmental Adaptation Biology, Ministry of Education, School of Life ScienceShandong UniversityQingdaoChina
  2. 2.Hunan Provincial Key Laboratory of Phytohormones, Southern Regional Collaborative Innovation Center for Grain and Oil CropsHunan Agricultural UniversityChangshaChina

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