Plant Growth Regulation

, Volume 86, Issue 2, pp 211–222 | Cite as

Characterization of the glutathione S-transferase (GST) gene family in Pyrus bretschneideri and their expression pattern upon superficial scald development

  • Libin WangEmail author
  • Ming Qian
  • Runze Wang
  • Li Wang
  • Shaoling ZhangEmail author
Original paper


Glutathione S-transferases (GSTs) proposedly play a crucial role in the development of superficial scald in pear fruit; however, the specific member from pear GST gene family, which plays an important role in this process, has not been identified until recently. In this study, a total of 62 GST family genes were identified in Pyrus bretschneideri genome, which were distributed across the 14 chromosomes and 8 scaffolds with an uneven distribution. They could be categorized into eight classes based on phylogenetic analysis, and WGD/segmental duplication mainly drove their expansion. The expression of PbrGSTs in ‘Yali’ pear fruit was tissue-specific. In accompany with superficial scald development was the accumulation of reactive oxygen species (ROS) accumulation and loss of ascorbic acid (AsA) in the pericarp of ‘Yali’ pear. Of 47 PbrGSTs detected in the pericarp, the transcription of 25 members were enhanced upon the development of superficial scald, while three in dehydroascorbate reductase (DHAR) class were downregulated in association with lower DHAR activity. In combination with the results of the impact of 1-MCP and MHO fumigation on the expression profile of PbrGSTs, PbrDHAR1, PbrDHAR2 and PbrDHAR4 were selected as the candidate gene involved in superficial scald development.


Evolution GST Low temperature stress Pear Physiological disorder 



We would like to thank the financial support to this study from the National Natural Science Foundation of China (31701868), China Postdoctoral Science Foundation (2017M620213 and 2017M621760), and the Fundamental Research Funds for the Central Universities (KJQN201813). Additionally, we thank Weiqi Luo (Horticultural Research Laboratory, Fort Pierce, Florida, USA) for providing some support with the statistical analysis.

Compliance with ethical standards

Conflict of interest

There has no conflict of interest among authors.

Supplementary material

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  1. Brown RE, Jarvis KL, Hyland KJ (1989) Protein measurement using bicinchoninic acid: elimination of interfering substances. Anal Biochem 180:136–139CrossRefPubMedGoogle Scholar
  2. Csiszár J, Horváth E, Váry Z, Gallé Á, Bela K, Brunner S, Tari I (2014) Glutathione transferase supergene family in tomato: salt stress-regulated expression of representative genes from distinct GST classes in plants primed with salicylic acid. Plant Physiol Biochem 78:15–26CrossRefGoogle Scholar
  3. Dong Y, Li C, Zhang Y, He Q, Daud MK, Chen J, Zhu S (2016) Glutathione S-transferase gene family in Gossypium raimondii and G. arboreum: Comparative genomic study and their expression under salt stress. Front Plant Sci. CrossRefPubMedCentralPubMedGoogle Scholar
  4. Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF (2008) Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet 42:443–461CrossRefPubMedGoogle Scholar
  5. Du L, Song J, Palmer LC, Fillmore S, Zhang Z (2017) Quantitative proteomic changes in development of superficial scald disorder and its response to diphenylamine and 1-MCP treatments in apple fruit. Postharvest Biol Technol 123:33–50CrossRefGoogle Scholar
  6. Gallé A, Csiszár J, Secenji M, Guóth A, Cseuz L, Tari I, Györgyey J, Erdei L (2009) Glutathione transferase activity and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance: response to water deficit. J Plant Physiol 166:1878–1891CrossRefPubMedGoogle Scholar
  7. Grabherr MG, Brian JH, Moran Y, Joshua ZL, Dawn AT, Ido A, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma FD, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652CrossRefPubMedPubMedCentralGoogle Scholar
  8. He G, Guan CN, Chen QX, Gou XJ, Liu W, Zeng QY, Lan T (2016) Genome-wide analysis of the glutathione S-transferase gene family in Capsella rubella: Identification, expression, and biochemical functions. Front Plant Sci. CrossRefPubMedCentralPubMedGoogle Scholar
  9. Hou Z, Hui W, Xu X, Guo Y (2013) Effects of MHO treatment on the development of superficial scald and reactive oxygen species metabolism in the apple peel. Acta Botanica Boreali-Occidentalia Sinica 33:1183–1189Google Scholar
  10. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297CrossRefPubMedPubMedCentralGoogle Scholar
  11. Hui W, Niu J, Xu X, Guan J (2016) Evidence supporting the involvement of MHO in the formation of superficial scald in ‘Dangshansuli’ pears. Postharvest Biol Technol 121:43–50CrossRefGoogle Scholar
  12. Jain M, Ghanashyam C, Bhattacharjee A (2010) Comprehensive expression analysis suggests overlapping and specific roles of rice glutathione S-transferase genes during development and stress responses. BMC Genomics. CrossRefPubMedCentralPubMedGoogle Scholar
  13. Jiang WK, Liu YL, Xia EH, Gao LZ (2013) Prevalent role of gene features in determining evolutionary fates of whole-genome duplication duplicated genes in flowering plants. Plant Physiol 161:1844–1861CrossRefPubMedPubMedCentralGoogle Scholar
  14. Kampranis SC, Damianova R, Atallah M, Toby G, Kondi G, Tsichlis PN, Makris AM (2000) A novel plant glutathione S-transferase/peroxidase suppresses Bax lethality in yeast. J Biol Chem 275:29207–29216CrossRefPubMedGoogle Scholar
  15. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870CrossRefGoogle Scholar
  17. Larrigaudière C, Candan AP, Giné-Bordonaba J, Civello M, Calvo G (2016) Unravelling the physiological basis of superficial scald in pears based on cultivar differences. Sci Hortic 213:340–345CrossRefGoogle Scholar
  18. Lee TH, Tang H, Wang X, Paterson AH (2013) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152–D1158CrossRefPubMedGoogle Scholar
  19. Lescot M, Patrice D, Gert T, Kathleen M, Yves M, Yves VP, Pierre R, Stephane R (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lurie S, Watkins CB (2012) Superficial scald, its etiology and control. Postharvest Biol Technol 65:44–60CrossRefGoogle Scholar
  21. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-SEq. Nat Methods 5:621–628CrossRefGoogle Scholar
  22. Nix DA, Eisen MB (2005) GATA: a graphic alignment tool for comparative sequence analysis. BMC Bioinform. CrossRefGoogle Scholar
  23. Qiao X, Li M, Li L, Yin H, Wu J, Zhang S (2015) Genome-wide identification and comparative analysis of the heat shock transcription factor family in Chinese white pear (Pyrus bretschneideri) and five other Rosaceae species. BMC Plant Biol. CrossRefPubMedCentralPubMedGoogle Scholar
  24. Qin A, Huang X, Zhang H, Wu J, Yang J, Zhang S (2015) Overexpression of PbDHAR2 from Pyrus sinkiangensis in transgenic tomato confers enhanced tolerance to salt and chilling stresses. HortScience 50:789–796Google Scholar
  25. Rao MV, Watkins CB, Brown SK, Weeden NF (1998) Active oxygen species metabolism in ‘White Angel’ × ‘Rome Beauty’ apple selections resistant and susceptible to superficial scald. J Am Soc Hortic Sci 123:299–304Google Scholar
  26. Rezaei MK, Shobbar ZS, Shahbazi M, Abedini R, Zare S (2013) Glutathione S-transferase (GST) family in barley: identification of members, enzyme activity, and gene expression pattern. J Plant Physiol 170:1277–1284CrossRefPubMedGoogle Scholar
  27. Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH, Singh KB (2009) The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant J 58:53–68CrossRefPubMedGoogle Scholar
  28. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28:231–234CrossRefPubMedPubMedCentralGoogle Scholar
  29. Song L, Wang J, Shafi M, Liu Y, Wang J, Wu J, Wu A (2016) Hypobaric treatment effects on chilling injury, mitochondrial dysfunction, and the ascorbate-glutathione (AsA-GSH) cycle in postharvest peach fruit. J Agr Food Chem 64:4665–4674CrossRefGoogle Scholar
  30. Sunkar R (2010) Plant stress tolerance: methods and protocols. Humana Press, New YorkCrossRefGoogle Scholar
  31. Tatarinova TV, Alexandrov NN, Bouck JB, Feldmann KA (2010) GC3 biology in corn, rice, sorghum and other grasses. BMC Genomics. CrossRefPubMedCentralPubMedGoogle Scholar
  32. Vilaplana R, Valentines MC, Toivonen P, Larrigaudière C (2006) Antioxidant potential and peroxidative state of ‘Golden Smoothee’ apples treated with 1-methylcyclopropene. J Am Soc Hortic Sci 131:104–109Google Scholar
  33. Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genom Proteom Bioinform 8:77–80CrossRefGoogle Scholar
  34. Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee T, Jin H, Marler B, Guo H, Kissinger J, Paterson A (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. CrossRefPubMedCentralPubMedGoogle Scholar
  35. Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi KJ, Huang XS, Wang YT, Zhao X, Wu JY, Deng C, Gou CY, Zhou WL, Yin H, Qin GH, Sha YH, Tao Y, Chen H, Yang YN, Song Y, Zhan DL, Wang J, Li LT, Dai MS, Gu C, Wang YZ, Shi DH, Wang XW, Zhang HP, Zeng L, Zheng DM, Wang CL, Chen MS, Wang GB, Xie L, Sovero V, Sha SF, Huang WJ, Zhang SJ, Zhang MY, Sun JM, Xu LL, Li Y, Liu X, Li QS, Shen JH, Wang JY, Paull RE, Bennetzen JL, Wang J, Zhang SL (2013) The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408CrossRefPubMedPubMedCentralGoogle Scholar
  36. Zhou H, Qi K, Liu X, Yin H, Wang P, Chen J, Wu J, Zhang S (2016) Genome-wide identification and comparative analysis of the cation proton antiporters family in pear and four other Rosaceae species. Mol Genet Genomics 291:1727–1742CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Centre of Pear Engineering Technology Research, State Key Laboratory of Crop Genetics and Germplasm EnhancementNanjing Agricultural UniversityNanjingChina

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