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Comparative proteomic analysis reveals the role of hydrogen sulfide in the adaptation of the alpine plant Lamiophlomis rotata to altitude gradient in the Northern Tibetan Plateau

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Abstract

Main conclusion

We found the novel role of hydrogen sulfide in the adaptation of the alpine plant to altitude gradient in the Northern Tibetan Plateau.

Alpine plants have developed strategies to survive the extremely cold conditions prevailing at high altitudes; however, the mechanism underlying the evolution of these strategies remains unknown. Hydrogen sulfide (H2S) is an essential messenger that enhances plant tolerance to environmental stress; however, its role in alpine plant adaptation to environmental stress has not been reported until now. In this work, we conducted a comparative proteomics analysis to investigate the dynamic patterns of protein expression in Lamiophlomis rotata plants grown at three different altitudes. We identified and annotated 83 differentially expressed proteins. We found that the levels and enzyme activities of proteins involved in H2S biosynthesis markedly increased at higher altitudes, and that H2S accumulation increased. Exogenous H2S application increased antioxidant enzyme activity, which reduced ROS (reactive oxygen species) damage, and GSNOR (S-nitrosoglutathione reductase) activity, which reduced RNS (reactive nitrogen species) damage, and activated the downstream defense response, resulting in protein degradation and proline and sugar accumulation. However, such defense responses could be reversed by applying H2S biosynthesis inhibitors. Based on these findings, we conclude that L. rotata uses multiple strategies to adapt to the alpine stress environment and that H2S plays a central role during this process.

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Abbreviations

APX:

Ascorbate peroxidase

CAS:

Beta-Cyanoalanine synthase

CAT:

Catalase

CBS:

Cystathionine b-synthase

CO:

Carbon monoxide

CSC:

Cysteine synthesis complex

CSE:

Cystathionine c lyase

D-CD:

d-Cysteine desulfhydrase

FDR:

False discovery rates

GSH:

Glutathione

GSNOR:

S-nitrosoglutathione reductase

H2S:

Hydrogen sulfide

D/L-CDs:

d/l-cysteine desulfhydrases

NO:

Nitric oxide

OAS:

O-acetyl serine

OAS-TL:

O-acetyl-thiol-serinelyase

ROS:

Reactive oxygen species

RNS:

Reactive nitrogen species

SOD:

Superoxide dismutase

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Acknowledgments

We thank the members of Yang Yongping’s group for their help during sample collection. This work was supported by the Young Academic and Technical Leader Raising Foundation of Yunnan Province (No. 2012HB041), the project of innovation team of Yunnan Province, the National Natural Sciences Foundation of China (No. 31170256), and the Major State Basic Research Development Program (2010CB951700).

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Correspondence to Yongping Yang or Xiangyang Hu.

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Supplemental Table S1 Ms/MS analysis of the differentially expressed protein spots (DOC 446 kb)

425_2014_2209_MOESM2_ESM.ppt

Supplemental Fig. S1 PCA analysis of the contribution of different environmental factors to the environmental stress response. a The contribution (in percentage points) of various principal components to plant biomass, as determined in our experiments. b The contribution (in degrees) of different environmental factors in principal component 1, as determined by PCA of our data (PPT 174 kb)

425_2014_2209_MOESM3_ESM.ppt

Supplemental Fig. S2 Biological replicates of 2D gels of samples harvested from altitudes of 4350, 4,800, and 5,200 m (PPT 6079 kb)

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Ma, L., Yang, L., Zhao, J. et al. Comparative proteomic analysis reveals the role of hydrogen sulfide in the adaptation of the alpine plant Lamiophlomis rotata to altitude gradient in the Northern Tibetan Plateau. Planta 241, 887–906 (2015). https://doi.org/10.1007/s00425-014-2209-9

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