Advertisement

Chloroplast proteomic analysis of Triticum aestivum L. seedlings responses to low levels of UV-B stress reveals novel molecular mechanism associated with UV-B tolerance

  • Limei GaoEmail author
  • Xiaofei Wang
  • Yongfeng Li
  • Rong Han
Research Article

Abstract

In this study, we have investigated UV-B-induced alterations including chloroplast ultrastructure, chlorophyll fluorescence parameters, physiological metabolism, and chloroplast proteome profile. Comparison of seedling phenotypic characterization and physiological status revealed that the low level of 1.08 KJ m−2 of UV-B irradiation had no obvious effects on seedling phenotype and growth and maintained better chloroplast ultrastructure and higher photosynthetic efficiency. Nevertheless, the high dose of 12.6 KJ m−2 of UV-B stress caused significant inhibitory effects on the growth and development of wheat seedlings. Proteomic analysis of chloroplasts with or without 1.08 KJ m−2 of UV-B irradiation identified 50 differentially expressed protein spots, of which 35 were further analyzed by MALDI-TOF/TOF mass spectrometry. These proteins were found to be involved in multiple cellular metabolic processes including ATP synthesis, light reaction, Calvin cycle, detoxifying and antioxidant reactions, protein metabolism, malate and tetrapyrrole biosynthesis, and signal transduction pathway. We also identified 3 novel UV-B-responsive proteins, spots 8801, 8802, and 9201, and predicted three new proteins might be UV-B protective proteins. Our results imply chloroplasts play a central protective role in UV-B resistance of wheat seedlings and also provide novel evidences that UV-B stress directly affects on the structure and function of chloroplasts and explore molecular mechanisms associated with plant UV-B tolerance from chloroplast perspective.

Keywords

Chloroplast proteomics UV-B stress Triticum aestivum L. seedlings MALDI-TOF/TOF mass spectrometry 

Notes

Acknowledgements

We thank Dr. Huiling Xu (The University of Melbourne, Australia) for critically reading the manuscript.

Funding information

This research was supported by Postgraduate Science and Technology Innovation Project of Shanxi Normal University (2017) and Shanxi Normal University Key Young Teacher Cultivation Project grant (Grant No. ZR1710).

References

  1. Armbruster U, Hertle A, Makarenko E, Zühlke J, Pribil M, Dietzmann A, Schliebner I, Aseeva E, Fenino E, Scharfenberg M, Voigt C, Leister D (2009) Chloroplast proteins without cleavable transit peptides: rare exceptions or a major constituent of the chloroplast proteome? Mol Plant 2:1325–1335CrossRefGoogle Scholar
  2. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  3. Casati P, Walbot V (2003) Gene expression profiling in response to ultraviolet radiation in maize genotypes with varying flavonoid content. Plant Physiol 132:1739–1754CrossRefGoogle Scholar
  4. Casati P, Walbot V (2004) Crosslinking of ribosomal proteins to RNA in maize ribosomes by UV-B and its effects on translation. Plant Physiol 136:3319–3332CrossRefGoogle Scholar
  5. Casati P, Zhang X, Burlingame AL, Walbot V (2005) Analysis of leaf proteome after UV-B irradiation in maize lines differing in sensitivity. Mol Cell Proteomics 4:1673–1685CrossRefGoogle Scholar
  6. Cembrowska-Lech D, Koprowski M, Kepczyński J (2015) Germination induction of dormant Avena fatua caryopses by KAR1 and GA3 involving the control of reactive oxygen species (H2O2 and O2 ·-) and enzymatic antioxidants (superoxide dismutase and catalase) both in the embryo and the aleurone layers. J Plant Physiol 176:169–179CrossRefGoogle Scholar
  7. Czégény G, Mátai A, Hideg É (2016) UV-B effects on leaves—oxidative stress and acclimation in controlled environments. Plant Sci 248:57–63CrossRefGoogle Scholar
  8. Darré M, Valerga L, Araque LCO, Lemoine ML, Demkura PV, Vicente AR, Concellón A (2017) Role of UV-B irradiation dose and intensity on color retention and antioxidant elicitation in broccoli florets (Brassica oleracea var. Italica). Postharvest Biol Technol 128:76–82CrossRefGoogle Scholar
  9. Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation mediated responses in plants Balancing damage and protection. Plant Physiol 133:1420–1428CrossRefGoogle Scholar
  10. Gao LM, Li YF, Han R (2015) He-Ne laser preillumination improves the resistance of tall fescue (Festuca arundinacea Schreb.) seedlings to high saline conditions. Protoplasma 252:1135–1148CrossRefGoogle Scholar
  11. Gao LM, Li YF, Shen ZH, Han R (2018) Responses of He-Ne laser on agronomic traits and the crosstalk between UVR8 signaling and phytochrome B signaling pathway in Arabidopsis thaliana subjected to supplementary ultraviolet-B (UV-B) stress. Protoplasma 255:761–771CrossRefGoogle Scholar
  12. He ZH, Li HW, Shen YK, Li ZS, Mi HL (2013) Comparative analysis of the chloroplast proteomes of a wheat (Triticum aestivum L.) single seed descent line and its parents. J Plant Physiol 170:1139–1147CrossRefGoogle Scholar
  13. Jansena MAK, Babu TS, Hellera D, Gaba V, Mattood AK, Edelmana M (1996) Ultraviolet-B effects on Spirodela oligorrhiza: induction of different protection mechanisms. Plant Sci 115:217–223CrossRefGoogle Scholar
  14. Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407–431CrossRefGoogle Scholar
  15. Kamal AHM, Cho K, Choi JS, Bae KH, Komatsu S, Uozumi N, Woo SH (2013) The wheat chloroplastic proteome. J Proteome 93:326–342CrossRefGoogle Scholar
  16. Khudyakova AY, Kreslavski VD, Shirshikova GN, Zharmukhamedov SK, Kosobryukhov AA, Allakhverdiev SI (2017) Resistance of Arabidopsis thaliana L. photosynthetic apparatus to UV-B is reduced by deficit of phytochromes B and A. J Photochem Photobiol B Biol 169:41–46CrossRefGoogle Scholar
  17. Kosmala A, Perlikowski D, Pawłowicz I, Rapacz M (2012) Changes in the chloroplast proteome following water deficit and subsequent watering in a high- and a low-drought-tolerant genotype of Festuca arundinacea. J Exp Bot 63:6161–6172CrossRefGoogle Scholar
  18. Kostina E, Wulff A, Julkunen-Tiitto R (2011) Growth, structure, stomatal responses and secondary metabolites of birch seedlings (Betula pendula) under elevated UV-B radiation in the field. Trees-Struct Funct 15:483–491CrossRefGoogle Scholar
  19. Król A, Weidner S (2017) Changes in the proteome of grapevine leaves (Vitis Vinifera L.) during long-term drought stress. J Plant Physiol 211:114–126CrossRefGoogle Scholar
  20. Lee HS (2000) Principles and experimental techniques of plant physiology and biochemistry (in Chinese), 1st edn. Higher Education Press, Beijing, ChinaGoogle Scholar
  21. Li YF, Gao LM, Han R (2016) A combination of He-Ne laser irradiation and exogenous NO application efficiently protect wheat seedling from oxidative stress caused by elevated UV-B stress. Environ Sci Pollut Res 23:23675–23682CrossRefGoogle Scholar
  22. Li YF, Gao LM, Han R (2017) He-Ne laser illumination ameliorates photochemical impairment in ultraviolet-B stressed-wheat seedlings via detoxifying ROS cytotoxicity. Russ J Plant Physiol 64:766–775CrossRefGoogle Scholar
  23. de Luna-Valdez LA, Martínez-Batallar AG, Hernández-Ortiz M, Encarnación-Guevara S, Ramos-Vega M, López-Bucio JS, León P, Guevara-García AA (2014) Proteomic analysis of chloroplast biogenesis (clb) mutants uncovers novel proteins potentially involved in the development of Arabidopsis thaliana chloroplasts. J Proteome 111:148–164CrossRefGoogle Scholar
  24. Ma M, Wang P, Yang RQ, Gu ZX (2018) Effects of UV-B radiation on the isoflavone accumulation and physiological-biochemical changes of soybean during germination. Food Chem 250:259–267CrossRefGoogle Scholar
  25. Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481CrossRefGoogle Scholar
  26. Mostek A, Borner A, Weidner S (2016) Comparative proteomic analysis of β-aminobutyric acid-mediated alleviation of salt stress in barley. Plant Physiol Biochem 99:150–161CrossRefGoogle Scholar
  27. Rahman MA, Alam I, Kim YG, Ahn NY, Heo SY, Lee DG, Liu GS, Lee BH (2015) Screening for salt-responsive proteins in two contrasting alfalfa cultivars using a comparative proteome approach. Plant Physiol Biochem 89:112–122CrossRefGoogle Scholar
  28. Rehman A, Rehman S, Khatoon A, Qasim M, Itoh T, Iwasaki Y, Wang X, Sunohara Y, Matsumoto H, Komatsu S (2018) Proteomic analysis of the promotive effect of plant-derived smoke on plant growth of chickpea. J Proteome 176:56–70CrossRefGoogle Scholar
  29. Shi LX, Teng SM (2013) The chloroplast protein import system: from algae to tree. BBA Mol Cell Res 1833:314–331Google Scholar
  30. Singh MK, Sharma JG, Chakrabarti R (2015) Simulation study of natural UV-B radiation on Catla catla and its impact on physiology, oxidative stress, Hsp 70 and DNA fragmentation. J Photochem Photobiol B Biol 149:156–163CrossRefGoogle Scholar
  31. Taalas P, Amanatidis GT, Heikkilä A (2000) European conference on atmospheric UV radiation: overview. J Geophys Res 105:4777–4785CrossRefGoogle Scholar
  32. Tamburino R, Vitale M, Ruggiero A, Sassi M, Sannino L, Arena S, Costa A, Batelli G, Zambrano N, Scaloni A, Grillo S, Scotti N (2017) Chloroplast proteome response to drought stress and recovery in tomato (Solanum lycopersicum L.). BMC Plant Biol 17:40CrossRefGoogle Scholar
  33. Taylor NL, Tan YF, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteome 72:367–378CrossRefGoogle Scholar
  34. Verdaguer D, Jansen MAK, Llorens L, Morales LO, Neugart S (2017) UV-A radiation effects on higher plants: exploring the known unknown. Plant Sci 255:72–81CrossRefGoogle Scholar
  35. Wang LX, Liang WY, Xing JH, Tan FL, Chen YY, Huang L, Cheng CL, Chen W (2013) Dynamics of chloroplast proteome in salt-stressed mangrove Kandelia candel (L.) Druce. J Proteome Res 12:5124–5136CrossRefGoogle Scholar
  36. Wang LX, Pan DZ, Li J, Tan FL, Hoffmann-Benning S, Liang WY, Chen W (2015) Proteomics analysis of changes in the Kandelia candel chloroplast proteins reveals pathways associated with salt tolerance. Plant Sci 231:159–172CrossRefGoogle Scholar
  37. Wu LC, Wang SX, Tian L, Wu LJ, Li MN, Zhang J, Li P, Zhang WQ, Chen YH (2018) Comparative proteomic analysis of the maize responses to early leaf senescence induced by preventing pollination. J Proteome 177:75–87CrossRefGoogle Scholar
  38. Xie YJ, Zhang W, Duan XL, Dai C, Zhang YH, Cui WT, Wang R, Shen WB (2015) Hydrogen-rich water-alleviated ultraviolet-B-triggered oxidative damage is partially associated with the manipulation of the metabolism of (iso) flavonoids and antioxidant defence in Medicago sativa. Funct Plant Biol 42:1141–1157CrossRefGoogle Scholar
  39. Yabu T, Todoriki S, Yamashita M (2001) Stress-induced apoptosis by heat shock, UV and γ-ray irradiation in zebrafish embryos detected by increased caspase activity and whole-mount TUNEL staining. Fish Sci 67:333–340CrossRefGoogle Scholar
  40. Zheng L, Su M, Wu X, Liu C, Qu C, Chen L, Huang H, Liu XQ, Hong FS (2008) Antioxidant stress is promoted by nano-anatase in spinach chloroplasts under UV-B radiation. Biol Trace Elem Res 121:69–79CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Limei Gao
    • 1
    • 2
    Email author
  • Xiaofei Wang
    • 2
  • Yongfeng Li
    • 3
  • Rong Han
    • 1
    • 2
  1. 1.Department of Biotechnology, College of Life ScienceShanxi Normal UniversityLinfenPeople’s Republic of China
  2. 2.Cell Biology Laboratory, College of Life ScienceShanxi Normal UniversityLinfenPeople’s Republic of China
  3. 3.Analysis and Testing CenterShanxi Normal UniversityLinfenPeople’s Republic of China

Personalised recommendations