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The role of nitric oxide signalling in response to salt stress in Chlamydomonas reinhardtii

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Abstract

Main conclusion

Nitric oxide signal and GSNOR activity play an essential role for Chlamydomonas reinhardtii response to salt stress.

The unicellular alga Chlamydomonas reinhardtii is one of the most important model organisms phylogenetically situated between higher plants and animals. In the present study, we used comparative proteomics and physiological approaches to study the mechanisms underlying the response to salt stress in C. reinhardtii. We identified 74 proteins that accumulated differentially after salt stress, including oxidative enzymes and enzymes associated with nitric oxide (NO) metabolism, cell damage, and cell autophagy processes. A set of antioxidant enzymes, as well as S-nitrosoglutathione reductase (GSNOR) activity, were induced to balance the cellular redox status during short-term salt stress. Enzymes involved in DNA repair and cell autophagy also contribute to adaptation to short-term salt stress. However, under long-term salt stress, antioxidant enzymes and GSNOR were gradually inactivated through protein S-nitrosylation, leading to oxidative damage and a reduction in cell viability. Modulating the protein S-nitrosylation levels by suppressing GSNOR activity or adding thioredoxin affected the plant’s adaptation to salt stress, through altering the redox status and DNA damage and autophagy levels. Based on these data, we propose that unicellular algae use multiple strategies to adapt to salt stress, and that, during this process, GSNOR activity and protein S-nitrosylation levels play important roles.

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Abbreviations

APX:

Ascorbate peroxidase

ATG:

Autophagy related protein

DHAR:

Dehydroascorbate reductase

GSNOR:

S-Nitrosoglutathione reductase

GST:

Glutathione S-transferase

MDHAR:

Monodehydroascorbate reductase

NO:

Nitric oxide

NR:

Nitrate reductase

cPTIO:

2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

SNO:

S-Nitrosothiol

TRXh5:

Thioredoxin-h5

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Acknowledgments

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for funding this Research Group NO (RG-1435-014).

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Correspondence to Xiangyang Hu or Aiqun Jia.

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425_2016_2528_MOESM1_ESM.pdf

Supplementary material 1 (PDF 5 kb) Suppl. Fig. S1 The effect of various concentrations of salt on the biomass of C. reinhardtii. The cells of were incubated in 100 ml liquid medium containing different concentrations of salt. After 3 days of culture, the biomass of C. reinhardtii was measured. Data represent the means of five replicate experiments (±SD)

425_2016_2528_MOESM2_ESM.pdf

Supplementary material 2 (PDF 5 kb) Suppl. Fig. S2 The degree of cell death in C. reinhardtii exposed to different concentrations of salt. The cells were incubated in 100 ml liquid medium containing different concentrations of salt. After 3 days of culture, the degree of cell death was measured using Evans Blue staining. Data represent the means of five replicate experiments (±SD)

425_2016_2528_MOESM3_ESM.pdf

Supplementary material 3 (PDF 401 kb) Suppl. Fig. S3 Biological replicates of 2D gels shown in Fig. 3a. Samples were collected after different periods of treatment with 100 mM NaCl

425_2016_2528_MOESM4_ESM.xls

Supplementary material 4 (XLS 182 kb) Suppl. Table S1 MS/MS analysis of protein spots that were differentially expressed in the C. reinhardtii cells treated with 100 mM NaCl

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Chen, X., Tian, D., Kong, X. et al. The role of nitric oxide signalling in response to salt stress in Chlamydomonas reinhardtii . Planta 244, 651–669 (2016). https://doi.org/10.1007/s00425-016-2528-0

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  • DOI: https://doi.org/10.1007/s00425-016-2528-0

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