Planta

, Volume 241, Issue 4, pp 887–906 | Cite as

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

  • Lan Ma
  • Liming Yang
  • Jingjie Zhao
  • Jingjing Wei
  • Xiangxiang Kong
  • Chuntao Wang
  • Xiaoming Zhang
  • Yongping Yang
  • Xiangyang Hu
Original Article

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.

Keywords

Adaptation H2Lamiophlomis Proteomics 

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

Notes

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).

Supplementary material

425_2014_2209_MOESM1_ESM.doc (446 kb)
Supplemental Table S1 Ms/MS analysis of the differentially expressed protein spots (DOC 446 kb)
425_2014_2209_MOESM2_ESM.ppt (178 kb)
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 (5.9 mb)
Supplemental Fig. S2 Biological replicates of 2D gels of samples harvested from altitudes of 4350, 4,800, and 5,200 m (PPT 6079 kb)

References

  1. Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669CrossRefPubMedCentralPubMedGoogle Scholar
  2. Alvarez C, Garcia I, Moreno I, Perez-Perez ME, Crespo JL, Romero LC, Gotor C (2012) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634CrossRefPubMedCentralPubMedGoogle Scholar
  3. Bai XG, Chen JH, Kong XX, Todd CD, Yang YP, Hu XY, Li DZ (2012) Carbon monoxide enhances the chilling tolerance of recalcitrant Baccaurea ramiflora seeds via nitric oxide-mediated glutathione homeostasis. Free Radic Biol Med 53:710–720CrossRefPubMedGoogle Scholar
  4. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240CrossRefPubMedGoogle Scholar
  5. Boehning D, Snyder SH (2003) Novel neural modulators. Annu Rev Neurosci 26:105–131CrossRefPubMedGoogle Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  7. Briggs AG, Bent AF (2011) Poly(ADP-ribosyl)ation in plants. Trends Plant Sci 16:372–380CrossRefPubMedGoogle Scholar
  8. Chen Q, Lauzon LM, DeRocher AE, Vierling E (1990) Accumulation, stability, and localization of a major chloroplast heat-shock protein. J Cell Biol 110:1873–1883CrossRefPubMedGoogle Scholar
  9. Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286CrossRefPubMedGoogle Scholar
  10. Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138:2233–2244CrossRefPubMedCentralPubMedGoogle Scholar
  11. Diz AP, Martinez-Fernandez M, Rolan-Alvarez E (2012) Proteomics in evolutionary ecology: linking the genotype with the phenotype. Mol Ecol 21:1060–1080CrossRefPubMedGoogle Scholar
  12. Foyer CH, Noctor G (2013) Redox signaling in plants. Antioxid Redox Signal 18:2087–2090CrossRefPubMedGoogle Scholar
  13. Garcia-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signalling. New Phytol 188:977–984CrossRefPubMedGoogle Scholar
  14. Gupta R, Deswal R (2012) Low temperature stress modulated secretome analysis and purification of antifreeze protein from Hippophae rhamnoides, a Himalayan wonder plant. J Proteome Res 11:2684–2696CrossRefPubMedGoogle Scholar
  15. Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee ? Plant Physiol Biochem 78:37–42CrossRefPubMedGoogle Scholar
  16. Hare PD, Cress WA, van Staden J (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50:413–434Google Scholar
  17. Herppich WB, Herppich M (1996) Ecophysiological investigations on plants of the genus Plectranthus (fam Lamiaceae) native to Yemen and southern Africa. Flora 191:401–408Google Scholar
  18. Kachroo A, Robin GP (2013) Systemic signaling during plant defense. Curr Opin Plant Biol 16:527–533CrossRefPubMedGoogle Scholar
  19. Kishor P, Hong Z, Miao GH, Hu C, Verma D (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394PubMedCentralPubMedGoogle Scholar
  20. Kong X, Ma L, Yang L, Chen Q, Xiang N, Yang Y, Hu X (2014) Quantitative proteomics analysis reveals that the nuclear cap-binding complex proteins Arabidopsis CBP20 and CBP80 modulate the salt stress response. J Proteome Res 13:2495–2510CrossRefPubMedGoogle Scholar
  21. Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  22. Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant, Cell Environ 36:1564–1572CrossRefGoogle Scholar
  23. Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19:998–1011CrossRefPubMedCentralPubMedGoogle Scholar
  24. Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464CrossRefPubMedCentralPubMedGoogle Scholar
  25. Lv X, Pu XJ, Qin GW, Zhu T, Lin HH (2014) The roles of autophagy in development and stress responses in Arabidopsis thaliana. Apoptosis 19:905–921CrossRefPubMedGoogle Scholar
  26. Mannuss A, Trapp O, Puchta H (2012) Gene regulation in response to DNA damage. Biochim Biophys Acta 1819:154–165CrossRefPubMedGoogle Scholar
  27. McCormack ML, Guo D (2014) Impacts of environmental factors on fine root lifespan. Front Plant Sci 5:205CrossRefPubMedCentralPubMedGoogle Scholar
  28. Mok YY, Atan MS, Yoke Ping C, Zhong Jing W, Bhatia M, Moochhala S, Moore PK (2004) Role of hydrogen sulphide in haemorrhagic shock in the rat: protective effect of inhibitors of hydrogen sulphide biosynthesis. Br J Pharmacol 143:881–889CrossRefPubMedCentralPubMedGoogle Scholar
  29. Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969CrossRefGoogle Scholar
  30. Riemenschneider A, Wegele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a d-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J 272:1291–1304CrossRefPubMedGoogle Scholar
  31. Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32:1151–1159CrossRefPubMedGoogle Scholar
  32. Scuffi D, Núñez Á, Laspina N, Gotor C, Lamattina L, Garcia-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate ABA-dependent stomatal closure. Plant Physiol. doi: 10.1104/pp.114.245373 PubMedGoogle Scholar
  33. Shen JJ, Xing TJ, Yuan HH, Liu ZQ, Jin ZP, Zhang LP, Pei YX (2013) Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS One 8:e77047CrossRefPubMedCentralPubMedGoogle Scholar
  34. Shi HT, Ye TT, Chan ZL (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74:99–107CrossRefPubMedGoogle Scholar
  35. Stone SL (2014) The role of ubiquitin and the 26S proteasome in plant abiotic stress signaling. Frontiers Plant Sci 5: 135; doi: 10.3389/fpls.2014.00135
  36. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell Environ 35:259–270CrossRefGoogle Scholar
  37. Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71:391–411CrossRefPubMedGoogle Scholar
  38. Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Signal Behav 3:525–536CrossRefPubMedCentralPubMedGoogle Scholar
  39. Valledor L, Jorrin J (2011) Back to the basics: maximizing the information obtained by quantitative two dimensional gel electrophoresis analyses by an appropriate experimental design and statistical analyses. J Proteomics 74:1–18CrossRefPubMedGoogle Scholar
  40. Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–718CrossRefPubMedGoogle Scholar
  41. Wilson PJ, Thompson K, Hodgson JG (1999) Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytol 143:155–162CrossRefGoogle Scholar
  42. Wirtz M, Hell R (2007) Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 19:625–639CrossRefPubMedCentralPubMedGoogle Scholar
  43. Wirtz M, Droux M, Hell R (2004) O-acetylserine (thiol) lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55:1785–1798CrossRefPubMedGoogle Scholar
  44. Wrzaczek M, Brosche M, Kangasjarvi J (2013) ROS signaling loops–production, perception, regulation. Curr Opin Plant Biol 16:575–582CrossRefPubMedGoogle Scholar
  45. Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S, Snyder SH, Wang R (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322:587–590CrossRefPubMedCentralPubMedGoogle Scholar
  46. Yang Y, Chen J, Liu Q, Ben C, Todd CD, Shi J, Yang Y, Hu X (2012) Comparative proteomic analysis of the thermotolerant plant Portulaca oleracea acclimation to combined high temperature and humidity stress. J Proteome Res 11:3605–3623CrossRefPubMedGoogle Scholar
  47. Yang LM, Tian DG, Todd CD, Luo YM, Hu XY (2013) Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J Proteome Res 12:1316–1330CrossRefPubMedGoogle Scholar
  48. Zhao C, Wang XQ, Yang FS (2014) Mechanisms underlying flower color variation in Asian species of Meconopsis: a preliminary phylogenetic analysis based on chloroplast DNA and anthocyanin biosynthesis genes. J Syst Evol 52:125–133CrossRefGoogle Scholar
  49. Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266CrossRefPubMedCentralPubMedGoogle Scholar
  50. Zhu Y, Dong AW, Shen WH (2012) Histone variants and chromatin assembly in plant abiotic stress responses. Biochim Biophys Acta 1819:343–348CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Lan Ma
    • 1
    • 2
    • 3
  • Liming Yang
    • 4
  • Jingjie Zhao
    • 1
    • 2
    • 3
  • Jingjing Wei
    • 1
    • 2
    • 3
  • Xiangxiang Kong
    • 1
    • 2
  • Chuntao Wang
    • 1
    • 2
  • Xiaoming Zhang
    • 1
    • 2
    • 3
  • Yongping Yang
    • 1
    • 2
    • 5
  • Xiangyang Hu
    • 1
    • 2
    • 5
  1. 1.Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of BotanyChinese Academy of ScienceKunmingChina
  2. 2.The Germplasm Bank of Wild Species, Kunming Institute of BotanyChinese Academy of SciencesKunmingChina
  3. 3.University of Chinese Academy of SciencesBeijingChina
  4. 4.School of Life Sciences, Jiangsu Key Laboratory for Eco-Agriculture Biotechnology Around Hongze LakeHuayin Normal UniversityHuai’anChina
  5. 5.Key Laboratory of Alpine Ecology and BiodiversityChinese Academy of SciencesBeijingChina

Personalised recommendations