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Hydrogen peroxide response in leaves of poplar (populus simonii × populus nigra) revealed from physiological and proteomic analyses

International Journal of Molecular Sciences (2017) 18(10)
DOI: 10.3390/ijms18102085
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Abstract

Hydrogen peroxide (H2O2) is one of the most abundant reactive oxygen species (ROS), which plays dual roles as a toxic byproduct of cell metabolism and a regulatory signal molecule in plant development and stress response. Populus simonii × Populus nigra is an important cultivated forest species with resistance to cold, drought, insect and disease, and also a key model plant for forest genetic engineering. In this study, H2O2 response in P. simonii × P. nigra leaves was investigated using physiological and proteomics approaches. The seedlings of 50-day-old P. simonii × P. nigra under H2O2 stress exhibited stressful phenotypes, such as increase of in vivo H2O2 content, decrease of photosynthetic rate, elevated osmolytes, antioxidant accumulation, as well as increased activities of several ROS scavenging enzymes. Besides, 81 H2O2-responsive proteins were identified in the poplar leaves. The diverse abundant patterns of these proteins highlight the H2O2-responsive pathways in leaves, including 14-3-3 protein and nucleoside diphosphate kinase (NDPK)-mediated signaling, modulation of thylakoid membrane structure, enhancement of various ROS scavenging pathways, decrease of photosynthesis, dynamics of proteins conformation, and changes in carbohydrate and other metabolisms. This study provides valuable information for understanding H2O2-responsive mechanisms in leaves of P. simonii × P. nigra.

Figures

  • Figure 1. The morphology changes of Populus simonii × Populus nigra under hydrogen peroxide (H2O2) stress. The aerial portion of 50-day-old seedling of P. simonii × P. nigra was immersed in 0, 12, 24 and 36 mM H2O2 for 6 h, respectively. Bar = 0.2 cm.
  • Figure 1. The morphology changes of Populus simonii × Populus nigra under hydrogen peroxide (H2O2) stress. The aerial portion of 50-day-old seedling of P. simonii × P. nigra was immersed in 0, 12, 24 and 36 mM H2O2 for 6 h, respectively. Bar = 0.2 cm.
  • Figure 3. e brane integrity and os olyte accu ulation in Populus simonii × Populus nigra leaves under H O2 treat ent: (A) alondialdehyde content; (B) relative electrolyte leakage; (C) proline content; (D) soluble sugar content; and (E) glycine betanine content. The values were determined after the plants were treated with 0, 12, 24 and 36 mM H2O2, and were presented as means ± SD (n = 3). The different small letters indicate significant difference (p < 0.05) among different treatments.
  • Figure 4. Activities of antioxidant enzymes and antioxidant contents in Populus simonii × Populus nigra leaves under H2O2 treatment: (A) H2O2 content and O2•− generation rate; (B) activities of superoxide dismutase (SOD) and catalase (CAT); (C) activities of ascorbate peroxidase (APX) and peroxidase (POD); (D) glutathione peroxidase (GPX) activity; (E) activities of onodehydroascorbate reductase (MDHAR) and dehydroascorbate reductase ( R); (F) activities of glutathione reductase (GR) and glutathione S-transferase (GST); (G) contents of ascorbate ( s ) an ehydroascorbate (DHA); and (H) contents of reduced glutathione (GSH) content a i i e l t t ione ( SSG) content. The values wer det rmined after plants were treated with 0, , 2O2, and were presented as means ± SD (n = 3). The differ i te significant di ference (p < 0.05) among differ nt treatments.
  • Figure 5. A representative 2DE gel images of proteins from leaves of Populus simonii × Populus nigra. Proteins were separated on 24 cm linear gradient immobilized pH gradient (IPG) strips (pH 4–7) using isoelectric focusing (IEF) in the first dimension, followed by 12.5% sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE) gels in the second dimension. The 2DE gel was stained with Coomassie Brilliant Blue. Molecular weight (MW) in kilodaltons (KDa) and isoelectric point (pI) of proteins are indicated on the left and top of the gel, respectively. Eighty-one H2O2responsive proteins identified by matrix-assisted laser desorption/ ionization (MALDI) tandem time of flight (TOF-TOF) mass spectrometry were marked with numbers on the gel, and the detailed information can be found in Table 1, Figure S1, and Tables S1.
  • Figure 7. Hierarchical clustering analysis of 81 H2O2-responsive proteins in leaves of Populus simonii × Populus nigra. The four columns represent different treatments, including 0, 12, 24 and 36 mM H2O2. The rows represent individual proteins. The increased or decreased proteins are indicated in red or green, respectively. The color intensity increases with increasing abundant differences, as shown in the scale bar. e scale bar indicates log (base2) transformed protein ndance ratios ranging from −1.8 to 1.8. Functional categories indicated by capital letters, s ot numbers, and protein names are listed on the right side. A, photosynthetic electron transfer chain; B, Calvin cycle; C, carbohydrate and energy metabolism; D, other metabolisms; E, protein synthesis; F, protein folding and unfolding; G, redox homeostasis and stress defense; H, signaling; I, cell structure; J, miscellaneous or function unknown. The abbreviations refer to Table 1.
  • Figure 8. The protein–protein interaction (PPI) network in Populus simonii × Populus nigra leaves revealed by STRING analysis. A total of 81 H2O2-responsive proteins represented by 59 unique homologous proteins from Arabidopsis are shown in PPI network. Six main groups are indicated in different colors. The PPI network is shown in the confidence view generated by STRING database. Stronger associations are represented by thicker lines. The abbreviations refer to Table 1.
  • Figure 9. Schematic presentation of H2O2-responsive mechanism in leaves of Populus simonii × Populus nigra. The identified proteins were integrated into subcellular pathways: (A) signaling; (B) cell structure; (C), redox homeostasis and stress defense; (D) photosynthetic electron transfer chain; (E) calvin cycle; (F) carbohydrate and energy metabolism; (G) amino acid metabolism; (H) tetrapyrrole biosynthesis; and (I) protein synthesis, folding and unfolding. The abundances of identified proteins (shaded in gray ovals), enzyme activities (shaded in yellow ovals), and substrate contents are marked with squares, circles and triangles in different colors, respectively. The increased and decreased proteins, enzyme activities, and substrate contents are represented in red and green, respectively. The color intensity increases with increasing differences. The solid line indicates single-step reaction, the dashed line indicates multistep reaction, and the dotted line indicates the movement of proteins or substances. The abbreviations of identified proteins refer to Table 1. The abbreviations of metabolites: 1,3-PGA, 1,3-bisphosphoglycerate; 2-PG, 2-phosphoglycerate; 3-IPM, 3-isopropylmalate; 3-PGA, 3- phosphoglycerate; 4-MOP, 4-methyl-2-oxopentanoate; ADP, adenosine diphosphate; ALA, 5-

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Yu, J., Jin, X., Sun, X., Gao, T., Chen, X., She, Y., … Dai, S. (2017). Hydrogen peroxide response in leaves of poplar (populus simonii × populus nigra) revealed from physiological and proteomic analyses. International Journal of Molecular Sciences, 18(10). https://doi.org/10.3390/ijms18102085

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