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Journal of Genetics

, 98:46 | Cite as

Transcriptome analysis of finger millet (Eleusine coracana (L.) Gaertn.) reveals unique drought responsive genes

  • M. S. Parvathi
  • Karaba N. NatarajaEmail author
  • Y. A. Nanja Reddy
  • Mahantesha B. N. Naika
  • M. V. Channabyre Gowda
Research Article
  • 68 Downloads

Abstract

Finger millet (Eleusine coracana (L.) Gaertn.), an important \(\hbox {C}_{4}\) species is known for its stress hardiness and nutritional significance. To identify novel drought responsive mechanisms, we generated transcriptome data from leaf tissue of finger millet, variety GPU-28, exposed to gravimetrically imposed drought stress so as to simulate field stress conditions. De novo assembly-based approach yielded 80,777 and 90,830 transcripts from well-irrigated (control) and drought-stressed samples, respectively. A total of 1790 transcripts were differentially expressed between the control and drought-stress treatments. Functional annotation and pathway analysis indicated activation of diverse drought-stress signalling cascade genes such as serine threonine protein phosphatase 2A (PP2A), calcineurin B-like interacting protein kinase31 (CIPK31), farnesyl pyrophosphate synthase (FPS), signal recognition particle receptor \(\upalpha \) (SRPR \(\alpha \)) etc. The basal regulatory genes such as TATA-binding protein (TBP)-associated factors (TAFs) were found to be drought responsive, indicating that genes associated with housekeeping or basal regulatory processes are activated under drought in finger millet. A significant portion of the expressed genes was uncharacterized, belonging to the category of proteins of unknown functions (PUFs). Among the differentially expressed PUFs, we attempted to assign putative function for a few, using a novel annotation tool, Proteins of Unknown Function Annotation Server. Analysis of PUFs led to the discovery of novel drought responsive genes such as pentatricopeptide repeat proteins and tetratricopeptide repeat proteins that serve as interaction modules in multiprotein interactions. The transcriptome data generated can be utilized for comparative analysis, and functional validation of the genes identified would be useful to understand the drought adaptive mechanisms operating under field conditions in finger millet, as has been already attempted for a few candidates such as CIPK31 and TAF6. Such an attempt is needed to enhance the productivity of finger millet under water-limited conditions, and/or to adopt the implicated mechanisms in other related crops.

Keywords

finger millet drought transcriptome ontology differentially expressed genes Eleusine coracana 

Notes

Acknowledgements

We acknowledge the Department of Biotechnology, Government of India, New Delhi for funding the adhoc project Phenomics and Genomics of Ragi (file no. BT/PR5791/AGR/2/852/2012; D.O. no. BT/AB/Climate/2007 (Part II)). This project is also partially funded by the Indian Council of Agricultural Research (AICRP-Small Millets), New Delhi, India. We also thank the Department of  Science and Technology, Government of India, for infrastructure support under DST-FIST programme. MS Parvathi would like to thank University Grants Commission, New Delhi, India for awarding Junior Research Fellowship (F. 17-3/2002 (SA-I)) during the course of the study.

Supplementary material

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References

  1. Agarwal S., Singh P. K. and Singh A. 2011 Responses of some genotypes of finger millet (Eleusine coracana Gaertn.) for their salt tolerance. Int. J. Curr. Res. 3, 45–50.Google Scholar
  2. Altschul S., Gish W., Miller W., Myers E. and Lipman D. 1990 Basic local alignment search tool. J. Mol. Biol. 215, 403–410.CrossRefGoogle Scholar
  3. Anders S. and Huber W. 2010 Differential expression analysis for sequence count data. Genome Biol. 11R, 106.CrossRefGoogle Scholar
  4. Andrews S. 2010 FastQC: a quality control tool for high throughput sequence data. Available online at http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
  5. Antolin-Llovera M., Leivar P., Arro M., Ferrer A., Boronat A. and Campos N. 2011 Modulation of plant HMG-CoA reductase by protein phosphatase 2A: positive and negative control at a key node of metabolism. Plant Signal Behav. 6, 1127–1131.CrossRefGoogle Scholar
  6. Apweiler R., Bairoch A., Wu C. H., Barker, W. C., Boeckmann B., Ferro S. et al. 2004 UniProt: the Universal Protein knowledgebase. Nucl. Acids Res. 32(Database issue), D115-9.Google Scholar
  7. Babitha K. C., Vemanna R. S., Nataraja K. N. and Udayakumar M. 2015 Overexpression of EcbHLH57 transcription factor from Eleusine coracana L. in tobacco confers tolerance to salt, oxidative and drought stress. PLoS One 10, e0137098.Google Scholar
  8. Benetka W., Koranda M., Maurer-Stroh S., Pittner F. and Eisenhaber F. 2006 Farnesylation or geranylgeranylation? Efficient assays for testing protein prenylation in vitro and in vivo. BMC Biochem. 7, 6.CrossRefGoogle Scholar
  9. Chinchilla D., Zipfel C., Robatzek S., Kemmerling B., Nurnberger T., Jones J. D. et al. 2007 A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500.CrossRefGoogle Scholar
  10. Dhanyalakshmi K. H., Naika M. B. N., Sajeevan R. S., Mathew O. K., Shafi K. M., Sowdhamini R. et al. 2016 An approach to function annotation for proteins of unknown function (PUFs) in the transcriptome of Indian mulberry. PLoS One 11, e0151323.CrossRefGoogle Scholar
  11. Eckert D., Andree N., Razanau A., Zock-Emmenthal S., Lutzelberger M., Plath S. et al. 2016 Prp4 kinase grants the license to splice: control of weak splice sites during spliceosome activation. PLoS Genet. 12, e1005768.CrossRefGoogle Scholar
  12. Grabherr M. G., Haas B. J., Yassour M., Levin J. Z., Thompson D. A., Amit I. et al. 2011 Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652.CrossRefGoogle Scholar
  13. Hatakeyama M., Aluri S., Balachadran M. T., Sivarajan S. R., Patrignani A., Grüter S. et al. 2018 Multiple hybrid de novo genome assembly of finger millet, an orphan allotetraploid crop. DNA Res. 25, 39–47.CrossRefGoogle Scholar
  14. Hilu K. 1994 Validation of the combination Eleusine coracana subspecies Africana (Kennedy-O’Byrne) Hilu et Dewet. Phytologia 76, 410–411.CrossRefGoogle Scholar
  15. Hilu K. W. and De Wet J. 1976 Domestication of Eleusine coracana. Econ. Bot. 30, 199–208.CrossRefGoogle Scholar
  16. Hittalmani S., Mahesh H. B., Shirke M. D., Biradar H., Uday G., Aruna Y. R. et al. 2017 Genome and transcriptome sequence of finger millet (Eleusine coracana (L.) Gaertn.) provides insights into drought tolerance and nutraceutical properties. BMC Genomics 18, 465.Google Scholar
  17. Jaiswal S., Antala T. J., Mandavia M. K., Chopra M., Jasrotia R. S., Tomar R. S. et al. 2018 Transcriptomic signature of drought response in pearl millet (Pennisetum glaucum (L.) and development of web-genomic resources. Sci. Rep. 8, 3382.Google Scholar
  18. Jiang Y., Cheng Z., Mandon E. C. and Gilmore R. 2008 An interaction between the SRP receptor and the translocon is critical during cotranslational protein translocation. J. Cell Biol. 180, 1149–1161.CrossRefGoogle Scholar
  19. Karaba A., Greco R., Aharoni A., Trijatmiko K. R., Marsch-Martinez N., Krishnan A. et al. 2007 Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc. Natl. Acad. Sci. USA 104, 15270–15275.CrossRefGoogle Scholar
  20. Keenan R. J., Freymann D. M., Stroud R. M. and Walter P. 2001 The signal recognition particle. Annu. Rev. Biochem. 70, 755–775.CrossRefGoogle Scholar
  21. Kumar H., Kawai T. and Akira S. 2011 Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30, 16–34.CrossRefGoogle Scholar
  22. Lago C., Clerici E., Mizzi L., Colombo L. and Kater M. M. 2004 TBP-associated factors in Arabidopsis. Gene 342, 231–241.CrossRefGoogle Scholar
  23. Levkau B., Koyama H., Raines E. W., Clurman B. E., Herren B., Orth K. et al. 1998 Cleavage of p21Cip1/Waf1 and p27Kip1 mediates apoptosis in endothelial cells through activation of Cdk2: role of a caspase cascade. Mol. Cell. 1, 553–563.CrossRefGoogle Scholar
  24. Manna S. 2015 An overview of pentatricopeptide repeat proteins and their applications. Biochimie 113, 93–99.CrossRefGoogle Scholar
  25. Moriya Y., Itoh M., Okuda S., Yoshizawa A. C. and Kanehisa M. 2007 KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35, W182–W185.CrossRefGoogle Scholar
  26. Nagarjuna K. N., Parvathi M. S., Sajeevan R. S., Pruthvi V., Mamrutha H. M. and Nataraja K. N. 2016 Full-length cloning and characterization of abiotic stress responsive CIPK31-like gene from finger millet, a drought-tolerant crop. Curr. Sci. 111, 890–894.CrossRefGoogle Scholar
  27. Naika M., Shameer K. and Sowdhamini R. 2013 Comparative analyses of stress-responsive genes in Arabidopsis thaliana: insight from genomic data mining, functional enrichment, pathway analysis and phenomics. Mol. Biosyst. 9, 1888–1908.CrossRefGoogle Scholar
  28. Nambara E. and McCourt P. 1999 Protein farnesylation in plants: a greasy tale. Curr. Opin. Plant Biol. 2, 388–392.CrossRefGoogle Scholar
  29. Pais S. M., Tellez-Inon M. T. and Capiati D. A. 2009 Serine/threonine protein phosphatases type 2A and their roles in stress signaling. Plant Signal Behav. 4, 1013–1015.CrossRefGoogle Scholar
  30. Parvathi M. S. 2010 Prospecting candidate genes for drought tolerance from finger millet (Eleusine coracana (L.) Gaertn). M.Sc. thesis, UAS Bengaluru, India.Google Scholar
  31. Parvathi M. S. and Nataraja K. N. 2017 Discovery of stress responsive TATA-box binding protein associated Factor6 (TAF6) from finger millet (Eleusine coracana (L.) Gaertn). J. Plant Biol. 60, 335–342.CrossRefGoogle Scholar
  32. Parvathi M. S., Nataraja K. N., Yashoda B. K., Ramegowda H. V., Mamrutha H. M. and Rama N. 2013 Expression analysis of stress responsive pathway genes linked to drought hardiness in an adapted crop, finger millet (Eleusine coracana). J. Plant Biochem. Biotechol. 22, 192–201.Google Scholar
  33. Qiu X. B., Ouyang S. Y., Li C. J., Miao S., Wang L. and Goldberg A. L. 2006 Hrpn13/ADRM1/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37. EMBO J. 25, 5742–5753.Google Scholar
  34. Rahman H., Jagadeeshselvam N., Valarmathi R., Sachin B., Sasikala R., Senthil N. et al. 2014 Transcriptome analysis of salinity responsiveness in contrasting genotypes of finger millet (Eleusine coracana L.) through RNA-sequencing. Plant Mol. Biol. 85, 485–503.CrossRefGoogle Scholar
  35. Rahman H., Ramanathan V., Nallathambi J., Duraialagaraja S. and Muthurajan R. 2016 Over-expression of a NAC67 transcription factor from finger millet (Eleusine coracana L.) confers tolerance against salinity and drought stress in rice. BMC Biotechnol. 16, 35.Google Scholar
  36. Rakshitha H. C. 2017 Studies on the role of TATA Box binding proteins (TBP) Associated Factors (TAFs) from finger millet in regulating abiotic stress acclimation response. M.Sc. thesis, UAS, Bengaluru, India.Google Scholar
  37. Ramegowda V., Senthil-Kumar M., Nataraja K. N., Reddy M. K., Mysore K. S. and Udayakumar M. 2012 Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance. PLoS One 7, e40397.CrossRefGoogle Scholar
  38. Senthil-Kumar M. and Udayakumar M. 2006 High-throughput virus-induced gene-silencing approach to assess the functional relevance of a moisture stress-induced cDNA homologous to Lea4. J. Exp. Bot. 57, 2291–2302.CrossRefGoogle Scholar
  39. Shailaja H. and Thirumeni S. 2007 Evaluation of salt-tolerance in finger millet (Eleusine coracana) genotypes at seedling stage. Indian J. Agric. Sci. 77, 672–674.Google Scholar
  40. Schuenemann D., Gupta S., Persello-Cartieaux F., Klimyuk V. I., Jones J. D., Nussaume L. et al. 1998 A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc. Natl. Acad. Sci. USA 95, 10312–10316.Google Scholar
  41. Taylor C. 1996 Farnesylation – a sticky business. Plant Cell 8, 2151–2153.PubMedCentralGoogle Scholar
  42. Thomas C. J., Kapoor M., Sharma S., Bausinger H., Zyilan U., Lipsker D. et al. 2002 Evidence of a trimolecular complex involving LPS, LPS binding protein and soluble CD14 as an effector of LPS response. FEBS Lett. 531, 184–188.CrossRefGoogle Scholar
  43. Tripathi V., Parasuraman B., Laxmi A. and Chattopadhyay D. 2009 CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J. 58, 778–790.CrossRefGoogle Scholar
  44. Upadhyaya H., Gowda C. and Reddy V. G. 2007 Morphological diversity in finger millet germplasm introduced from southern and Eastern Africa. J. SAT Agric. Res. 3, 1–3.Google Scholar
  45. Vetriventhan M., Upadhyaya H. D., Dwivedi S. L., Pattanashetti S. K. and Singh S. K. 2015 Finger and foxtail millets. In: Genetic and genomic resources for grain cereals improvement (ed. Mohar Singh and Hari D. Upadhyaya), pp. 291–319. Academic Press, Elsevier.Google Scholar
  46. Walter P. and Johnson A. E. 1994 Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10, 87–119.CrossRefGoogle Scholar
  47. Xiang Y., Huang Y. and Xiong L. 2007 Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol. 144, 1416–1428.CrossRefGoogle Scholar
  48. Zeytuni N. and Zarivach R. 2012 Structural and functional discussion of the tetra-trico-peptide repeat, a protein interaction module. Structure 20, 397–405.CrossRefGoogle Scholar
  49. Zhang H., Yang B., Liu W. Z., Li H., Wang L., Wang B. et al. 2014 Identification and characterization of CBL and CIPK gene families in canola (Brassica napus L.). BMC Plant Biol. 14, 8.Google Scholar

Copyright information

© Indian Academy of Sciences 2019

Authors and Affiliations

  • M. S. Parvathi
    • 1
  • Karaba N. Nataraja
    • 1
    Email author
  • Y. A. Nanja Reddy
    • 1
    • 2
  • Mahantesha B. N. Naika
    • 1
    • 3
  • M. V. Channabyre Gowda
    • 2
  1. 1.Department of Crop PhysiologyUniversity of Agricultural SciencesBengaluru India
  2. 2.AICRP (Small Millets)ICAR-UASBengaluru India
  3. 3.Department of Biotechnology and Crop Improvement, K.R.C. College of HorticultureUniversity of Horticultural SciencesBagalkot India

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