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Genome-wide analysis of glutathione S-transferase gene family in chickpea suggests its role during seed development and abiotic stress

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Abstract

Glutathione S-transferases (GSTs) are multifunctional proteins that help in oxidative stress metabolism and detoxification of xenobiotic compounds. Studies pertaining to GST gene family have been undertaken in various plant species, however no information is available with respect to GST genes in chickpea. In the current study, we identified a total of 51 GST encoding genes in chickpea (CaGST) genome. Phylogenetic analysis revealed that GST gene family can be divided into eleven distinct classes. Tau and phi were the major classes in chickpea and one third of the CaGST genes represented segmental duplication and purifying selection was common among these genes. Expression of many CaGST genes, in particular, members of tau class were found to be upregulated under abiotic stress conditions. In addition, CaGST genes displayed differential expression patterns across diverse organs/tissues, suggesting their roles in developmental processes. Many CaGST genes showed opposite expression pattern in small- and large-seeded chickpea cultivars during seed development. Higher expression of CaGST genes in small-seeded cultivar at maturation stages of seed development suggested their important role in seed development and seed size/weight determination in chickpea. Overall, these results provide a comprehensive information on GST gene family members in chickpea and is expected to provide a rational platform to explore versatile role of these genes in semi-arid legume crops.

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References

  1. Edwards R, Dixon DP (2005) Plant glutathione transferases. Methods Enzymol 401:169–186

    Article  CAS  PubMed  Google Scholar 

  2. Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmcol Toxicol 45:51–88

    Article  CAS  Google Scholar 

  3. Coleman JOD, Blake-Kalff MMA, Davies TGE (1997) Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation. Trends Plant Sci 2:144–151

    Article  Google Scholar 

  4. Dixon DP, Edwards R (2010) Roles for stress-inducible lambda glutathione transferases in flavonoid metabolism in plants as identified by ligand fishing. J Biol Chem 285:36322–36329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ding N, Wang A, Zhang X et al (2017) Identification and analysis of glutathione S-transferase gene family in sweet potato reveal divergent GST-mediated networks in aboveground and underground tissues in response to abiotic stresses. BMC Plant Biol 17:1–15

    Article  CAS  Google Scholar 

  6. Islam S, Rahman IA, Islam T, Ghosh A (2017) Genome-wide identification and expression analysis of glutathione S-transferase gene family in tomato: gaining an insight to their physiological and stress-specific roles. PLoS ONE 12:1–28

    CAS  Google Scholar 

  7. 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 Genom 11:1–17

    Article  CAS  Google Scholar 

  8. Kayum MA, Nath UK, Park JI et al (2018) Genome-wide identification, characterization, and expression profiling of glutathione S-transferase (GST) family in pumpkin reveals likely role in cold-stress tolerance. Genes (Basel) 9:1–21

    Google Scholar 

  9. Khan N, Hu CM, Amjad Khan W, Hou X (2018) Genome-wide identification, classification, and expression divergence of glutathione-transferase family in Brassica rapa under multiple hormone treatments. Biomed Res Int 2018:6023457

    PubMed  PubMed Central  Google Scholar 

  10. Lan T, Yang ZL, Yang X et al (2009) Extensive functional diversification of the populus glutathione S-transferase supergene family. Plant Cell 21:3749–3766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Liu YJ, Han XM, Ren LL et al (2013) Functional divergence of the glutathione S-transferase supergene family in Physcomitrella patens reveals complex patterns of large gene family evolution in land plants. Plant Physiol 161:773–786

    Article  CAS  PubMed  Google Scholar 

  12. Sappl PG, Carroll AJ, Clifton R et al (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 58:53–68

    Article  CAS  PubMed  Google Scholar 

  13. Dong Y, Li C, Zhang Y et al (2016) Glutathione s-transferase gene family in Gossypium raimondii and G. arboreum: comparative genomic study and their expression under salt stress. Front Plant Sci 7:1–16

    CAS  Google Scholar 

  14. Wang L, Qian M, Wang R et al (2018) Characterization of the glutathione S-transferase (GST) gene family in Pyrus bretschneideri and their expression pattern upon superficial scald development. Plant Growth Regul 86:211–222

    Article  CAS  Google Scholar 

  15. Oakley AJ (2005) Glutathione transferases: new functions. Curr Opin Struct Biol 15:716–723

    Article  CAS  PubMed  Google Scholar 

  16. Nianiou-Obeidat I, Madesis P, Kissoudis C et al (2017) Plant glutathione transferase-mediated stress tolerance: functions and biotechnological applications. Plant Cell Rep 36:791–805

    Article  CAS  PubMed  Google Scholar 

  17. Du J, Ren J, Ye X et al (2018) Genome-wide identification and expression analysis of the glutathione S-transferase (GST) family under different developmental tissues and abiotic stresses in Chinese cabbage (Brassica rapa ssp. pekinensis). PeerJ Preprints 6:e26629v1

    Google Scholar 

  18. Gullner G, Komives T, Király L, Schröder P (2018) Glutathione S-transferase enzymes in plant-pathogen interactions. Front Plant Sci 9:1836

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kumar S, Trivedi PK (2018) Glutathione S-transferases: role in combating abiotic stresses including arsenic detoxification in plants. Front Plant Sci 9:1–9

    Article  Google Scholar 

  20. Wahibah NN, Tsutsui T, Tamaoki D et al (2018) Expression of barley glutathione s-transferase13 gene reduces accumulation of reactive oxygen species by trichothecenes and paraquat in arabidopsis plants. Plant Biotechnol 35:71–79

    Article  CAS  Google Scholar 

  21. Karavangeli M, Labrou NE, Clonis YD, Tsaftaris A (2005) Development of transgenic tobacco plants overexpressing maize glutathione S-transferase I for chloroacetanilide herbicides phytoremediation. Biomol Eng 22:121–128

    Article  CAS  PubMed  Google Scholar 

  22. Benekos K, Kissoudis C, Nianiou-Obeidat I et al (2010) Overexpression of a specific soybean GmGSTU4 isoenzyme improves diphenyl ether and chloroacetanilide herbicide tolerance of transgenic tobacco plants. J Biotechnol 150:195–201

    Article  CAS  PubMed  Google Scholar 

  23. Jha B, Sharma A, Mishra A (2011) Expression of SbGSTU (tau class glutathione S-transferase) gene isolated from Salicornia brachiata in tobacco for salt tolerance. Mol Biol Rep 38:4823–4832

    Article  CAS  PubMed  Google Scholar 

  24. Sharma R, Sahoo A, Devendran R, Jain M (2014) Over-expression of a rice tau class glutathione S-transferase gene improves tolerance to salinity and oxidative stresses in Arabidopsis. PLoS ONE 9:1–11

    Google Scholar 

  25. Srivastava D, Verma G, Chauhan AS et al (2019) Rice (Oryza sativa L.) tau class glutathione S-transferase (OsGSTU30) overexpression in Arabidopsis thaliana modulates a regulatory network leading to heavy metal and drought stress tolerance. Metallomics 11:375–389

    Article  CAS  PubMed  Google Scholar 

  26. Dean JD, Goodwin PH, Hsiang T (2005) Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 56:1525–1533

    Article  CAS  PubMed  Google Scholar 

  27. Xu J, Tian YS, Xing XJ et al (2016) Over-expression of AtGSTU19 provides tolerance to salt, drought and methyl viologen stresses in Arabidopsis. Physiol Plant 156:164–175

    Article  CAS  PubMed  Google Scholar 

  28. Ryu HY, Kim SY, Park HM et al (2009) Modulations of AtGSTF10 expression induce stress tolerance and BAK1-mediated cell death. Biochem Biophys Res Commun 379:417–422

    Article  CAS  PubMed  Google Scholar 

  29. Marrs KA, Alfenito MR, Lloyd AM, Walbot V (1995) A glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375:397–400

    Article  CAS  PubMed  Google Scholar 

  30. Mueller LA, Goodman CD, Silady RA, Walbot V (2000) Required for anthocyanin sequestration, is a flavonoid-binding protein 1. Society 123:1561–1570

    CAS  Google Scholar 

  31. Sun Y, Li H, Huang JR (2012) Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Mol Plant 5:387–400

    Article  CAS  PubMed  Google Scholar 

  32. Roxas VP, Lodhi SA, Garrett DK et al (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41:1229–1234

    Article  CAS  PubMed  Google Scholar 

  33. Xu J, Xing XJ, Tian YS et al (2015) Transgenic Arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLoS ONE 10:1–16

    Google Scholar 

  34. Moons A (2005) Regulatory and functional interactions of plant growth regulators and plant glutathione S-Transferases (GSTs). Vitam Horm 72:155–202

    Article  CAS  PubMed  Google Scholar 

  35. Basantani M, Srivastava A (2007) Plant glutathione transferases—a decade falls short. Can J Bot 85:443–456

    Article  CAS  Google Scholar 

  36. French CE, Bell JML, Ward FB (2008) Diversity and distribution of hemerythrin-like proteins in prokaryotes. FEMS Microbiol Lett 279:131–145

    Article  CAS  PubMed  Google Scholar 

  37. Mano J, Kanameda S, Kuramitsu R et al (2019) Detoxification of reactive carbonyl species by glutathione transferase tau isozymes. Front Plant Sci 10:1–7

    Article  Google Scholar 

  38. Varshney RK, Song C, Saxena RK et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246

    Article  CAS  PubMed  Google Scholar 

  39. Chi Y, Cheng Y, Vanitha J et al (2011) Expansion mechanisms and functional divergence of the glutathione S-transferase family in sorghum and other higher plants. DNA Res 18:1–16

    Article  CAS  PubMed  Google Scholar 

  40. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hu B, Jin J, Guo AY et al (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  42. Wang Y, Tang H, Debarry JD et al (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:1–14

    Article  CAS  Google Scholar 

  43. Singh VK, Garg R, Jain M (2013) A global view of transcriptome dynamics during flower development in chickpea by deep sequencing. Plant Biotechnol J 11:691–701

    Article  CAS  PubMed  Google Scholar 

  44. Jain M, Misra G, Patel RK et al (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729

    Article  CAS  PubMed  Google Scholar 

  45. Garg R, Bhattacharjee A, Jain M (2015) Genome-scale transcriptomic insights into molecular aspects of abiotic stress responses in chickpea. Plant Mol Biol Rep 33:388–400

    Article  CAS  Google Scholar 

  46. Garg R, Singh VK, Rajkumar MS et al (2017) Global transcriptome and coexpression network analyses reveal cultivar-specific molecular signatures associated with seed development and seed size/weight determination in chickpea. Plant J 91:1088–1107

    Article  CAS  PubMed  Google Scholar 

  47. Garg R, Sahoo A, Tyagi AK, Jain M (2010) Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem Biophys Res Commun 396:283–288

    Article  CAS  PubMed  Google Scholar 

  48. Wagner U, Edwards R, Dixon DP, Mauch F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515–532

    Article  CAS  PubMed  Google Scholar 

  49. Han XM, Yang ZL, Liu YJ et al (2018) Genome-wide profiling of expression and biochemical functions of the Medicago glutathione S-transferase gene family. Plant Physiol Biochem 126:126–133

    Article  CAS  PubMed  Google Scholar 

  50. Vaish S, Awasthi P, Tiwari S et al (2018) In silico genome-wide identification and characterization of the glutathione S-transferase gene family in Vigna radiata. Genome 61:311–322

    Article  CAS  PubMed  Google Scholar 

  51. Thom R, Cummins I, Dixon DP et al (2002) Structure of a tau class glutathione S-transferase from wheat active in herbicide detoxification. Biochemistry 41:7008–7020

    Article  CAS  PubMed  Google Scholar 

  52. Board PG, Coggan M, Chelvanayagam G et al (2000) Identification, characterization, and crystal structure of the omega class glutathione transferases. J Biol Chem 275:24798–24806

    Article  CAS  PubMed  Google Scholar 

  53. Flagel LE, Jonathan FW (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183:557–564

    Article  PubMed  Google Scholar 

  54. Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38:615–643

    Article  CAS  PubMed  Google Scholar 

  55. Jia B, Sun M, Sun X et al (2016) Overexpression of GsGSTU13 and SCMRP in Medicago sativa confers increased salt-alkaline tolerance and methionine content. Physiol Plant 156:176–189

    Article  CAS  PubMed  Google Scholar 

  56. Kissoudis C, Kalloniati C, Flemetakis E et al (2015) Stress-inducible GmGSTU4 shapes transgenic tobacco plants metabolome towards increased salinity tolerance. Acta Physiol Plant 37:102

    Article  CAS  Google Scholar 

  57. George S, Venkataraman G, Parida A (2010) A chloroplast-localized and auxin-induced glutathione S-transferase from phreatophyte Prosopis juliflora confer drought tolerance on tobacco. J Plant Physiol 167:311–318

    Article  CAS  PubMed  Google Scholar 

  58. Seppänen MM, Cardi T, Borg Hyökki M, Pehu E (2000) Characterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S. tuberosum and their interspecific somatic hybrids. Plant Sci 153:125–133

    Article  PubMed  Google Scholar 

  59. Anderson JV, Davis DG (2004) Abiotic stress alters transcript profiles and activity of glutathione S-transferase, glutathione peroxidase, and glutathione reductase in Euphorbia esula. Physiol Plant 120:421–433

    Article  CAS  PubMed  Google Scholar 

  60. Tsuchiya T, Takesawa T, Kanzaki H, Nakamura I (2004) Genomic structure and differential expression of two tandem-arranged GSTZ genes in rice. Gene 335:141–149

    Article  CAS  PubMed  Google Scholar 

  61. Vijayakumar H, Thamilarasan SK, Shanmugam A et al (2016) Glutathione transferases superfamily: cold-inducible expression of distinct GST genes in Brassica oleracea. Int J Mol Sci 17:1211

    Article  PubMed Central  CAS  Google Scholar 

  62. Gallé Á, Csiszár J, Secenji M et al (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 166:1878–1891

    Article  PubMed  CAS  Google Scholar 

  63. Rezaei MK, Shobbar ZS, Shahbazi M et al (2013) Glutathione S-transferase (GST) family in barley: identification of members, enzyme activity, and gene expression pattern. J Plant Physiol 170:1277–1284

    Article  CAS  PubMed  Google Scholar 

  64. Sun W, Xu X, Zhu H et al (2010) Comparative transcriptomic profiling of a salt-tolerant wild tomato species and a salt-sensitive tomato cultivar. Plant Cell Physiol 51:997–1006

    Article  CAS  PubMed  Google Scholar 

  65. Kumar S, Asif MH, Chakrabarty D et al (2013) Expression of a rice Lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. J Hazard Mater 248–249:228–237

    Article  PubMed  CAS  Google Scholar 

  66. Chan C, Lam HM (2014) A putative lambda class glutathione S-transferase enhances plant survival under salinity stress. Plant Cell Physiol 55:570–579

    Article  CAS  PubMed  Google Scholar 

  67. Islam MS, Choudhury M, Majlish ANK et al (2018) Comprehensive genome-wide analysis of glutathione S-transferase gene family in potato (Solanum tuberosum L.) and their expression profiling in various anatomical tissues and perturbation conditions. Gene 639:149–162

    Article  CAS  PubMed  Google Scholar 

  68. Gallé Á, Czékus Z, Bela K et al (2018) Diurnal changes in tomato glutathione transferase activity and expression: short communication. Acta Biol Hung 69:505–509

    Article  PubMed  CAS  Google Scholar 

  69. Yang Q, Han XM, Gu JK et al (2019) Functional and structural profiles of GST gene family from three Populus species reveal the sequence–function decoupling of orthologous genes. New Phytol 221:1060–1073

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work is financially supported by the Department of Biotechnology (DBT), Government of India, under the Challenge Programme on Chickpea Functional Genomics (BT/AGR/CG-PhaseII/01/2014). The infrastructural facilities provided by Jawaharlal Nehru University, New Delhi, India, are gratefully acknowledged.

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  1. Rajesh Ghangal and Mohan Singh Rajkumar contributed equally.

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  1. School of Computational & Integrative Sciences, Jawaharlal Nehru University, New Delhi, 110067, India

    Rajesh Ghangal, Mohan Singh Rajkumar & Mukesh Jain

  2. Department of Life Sciences, School of Natural Sciences, Shiv Nadar University, Gautam Buddha Nagar, Dadri, India

    Rohini Garg

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  1. Rajesh Ghangal
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Correspondence to Mukesh Jain.

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Ghangal, R., Rajkumar, M.S., Garg, R. et al. Genome-wide analysis of glutathione S-transferase gene family in chickpea suggests its role during seed development and abiotic stress. Mol Biol Rep 47, 2749–2761 (2020). https://doi.org/10.1007/s11033-020-05377-8

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