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Transcriptomes of Indian barnyard millet and barnyardgrass reveal putative genes involved in drought adaptation and micronutrient accumulation

  • Murukarthick Jayakodi
  • Manimekalai Madheswaran
  • Karthikeyan Adhimoolam
  • Sampath Perumal
  • Dhasarathan Manickam
  • Thangaraj Kandasamy
  • Tae-Jin YangEmail author
  • Senthil NatesanEmail author
Original Article

Abstract

Indian barnyard millet (Echinochloa frumentacea) is a rich source of dietary fiber, minerals and protein. The lack of genetic resources has slowed the discovery of genes involved in its nutrient accumulation and climate resilience. Here, we present the first transcriptomes of E. frumentacea [97,065 transcripts, including 65,276 protein-coding transcripts, over 90% of which have been functionally annotated, and 31,789 long noncoding RNA (lncRNA) transcripts] and its wild relative E. crus-galli (93,725 transcripts, including 68,480 protein-coding transcripts, 89% of which have been annotated). Comparative transcriptome analysis identified 4159 protein-coding and 2258 lncRNA transcripts in Indian barnyard millet that showed either up- or down-regulated expression when compared with E. crus-galli, and 3489 protein-coding transcripts unique to Indian barnyard millet were also detected. Additional analysis revealed that photosynthesis is likely crucial in the drought adaptation of Indian barnyard millet. We then identified possible genes regulation responsible for drought tolerance and Fe and Zn accumulation. Moreover, based on the simple sequence repeat (SSR)-containing sequence, 30 SSR primer pairs were arbitrarily selected, synthesized and used to screen the 30 E. frumentacea accessions. Of these, 10 SSR primers were polymorphic. Collectively, our results enhance the knowledge of micronutrient accumulation and drought tolerance in Indian barnyard millet, as well as of the genetic diversity of Echinochloa species.

Keywords

Drought Simple sequence repeats Indian barnyard millet Micronutrients 

Notes

Acknowledgements

All the authors wish to acknowledge National Agricultural Development Programme (NADP)/Rashtriya Krishi Vikas Yojana (RKVY)—Tamil Nadu Govt, for providing financial support. Thanks to Centre of Innovation (CI), Agricultural College and Research Institute, Tamil Nadu Agricultural University, Madurai, for providing instrumentation facilities.

Compliance with ethical standards

Conflict of interest

The authors have declared that no competing, or conflicts of interest exist.

Supplementary material

11738_2019_2855_MOESM1_ESM.xlsx (32 kb)
Supplementary file1 (XLSX 32 kb)
11738_2019_2855_MOESM2_ESM.doc (1.5 mb)
Supplementary file2 (DOC 1540 kb)

References

  1. Benoist BD, McLean E, Egli I, Cogswell M (eds) (2008) Worldwide prevalence of anaemia 1993–2005: WHO global database on anaemia. World Health Organization, GenevaGoogle Scholar
  2. Chandel G, Samuel P, Dubey M, Meena R (2011) In silico expression analysis of QTL specific candidate genes for grain micronutrient (Fe/Zn) content using ESTs and MPSS signature analysis in rice (Oryza sativa L.). J Plant Genet Transgenics 2:11–22Google Scholar
  3. Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412CrossRefGoogle Scholar
  4. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatic 21:3674–3676CrossRefGoogle Scholar
  5. Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  6. Garg R, Patel RK, Tyagi AK, Jain M (2011) De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Res 18:53–63CrossRefGoogle Scholar
  7. Gimode D, Odeny DA, de Villiers EP, Wanyonyi S, Dida MM, Mneney EE, Muchugi A, Machuka J, de Villiers SM (2016) Identification of SNP and SSR markers in finger millet using next generation sequencing technologies. PloS One 11:e0159437CrossRefGoogle Scholar
  8. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, 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 29:644–652CrossRefGoogle Scholar
  9. Hadimani NA, Malleshi NG (1993) Studies on milling, physico-chemical properties, nutrient composition and dietary fibre content of millets. J Food Sci Technol 30:17–20Google Scholar
  10. Han XJ, Wang YD, Chen YC, Lin LY, Wu QK (2013) Transcriptome sequencing and expression analysis of terpenoid biosynthesis genes in Litsea cubeba. PloS one 8:e76890CrossRefGoogle Scholar
  11. Jayakodi M, Lee SC, Lee YS, Park HS, Kim NH, Jang W, Lee HO, Joh HJ, Yan TJ (2015) Comprehensive analysis of Panax ginseng root transcriptomes. BMC Plant Biol 15:138CrossRefGoogle Scholar
  12. Jin T, Chen J, Zhu L, Zhao Y, Guo J, Huang Y (2015) Comparative mapping combined with homology-based cloning of the rice genome reveals candidate genes for grain zinc and iron concentration in maize. BMC Genet 16:17CrossRefGoogle Scholar
  13. Jo Y, Lian S, Cho JK, Choi H, Kim SM, Kim SL, Lee BC, Cho WK (2016) De novo transcriptome assembly of Setaria italica variety Taejin. Genom Data 8:121–122CrossRefGoogle Scholar
  14. Kalia RK, Rai MK, Kalia S, Singh R, Dhawan A (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177:309–334CrossRefGoogle Scholar
  15. Kopylova E, Noé L, Touzet H (2012) SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics 28:3211–3217CrossRefGoogle Scholar
  16. Kotecha PV (2008) Micronutrient malnutrition in India: let us say “no” to it now. Indian J Community Med 33:9–10CrossRefGoogle Scholar
  17. Kumar A, Gaur VS, Goel A, Gupta AK (2015) De novo assembly and characterization of developing spikes transcriptome of finger millet (Eleusine coracana): a minor crop having nutraceutical properties. Plant Mol Biol Rep 33:905–922CrossRefGoogle Scholar
  18. Kumari SK, Thayumanavan B (1997) Comparative study of resistant starch from minor millets on intestinal responses, blood glucose, serum cholesterol and triglycerides in rats. J Food Sci Technol 75:296–302Google Scholar
  19. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323CrossRefGoogle Scholar
  20. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760CrossRefGoogle Scholar
  21. Li J, Liu B, Cheng F, Wang X, Aarts MG, Wu J (2014) Expression profiling reveals functionally redundant multiple-copy genes related to zinc, iron and cadmium responses in Brassica rapa. New Phyto 203:182–194CrossRefGoogle Scholar
  22. Mabberley DJ (1997) The plant book: a portable dictionary of the vascular plants. Cambridge University Press, Cambridge, p 858Google Scholar
  23. Manimekalai M, Dhasarathan M, Karthikeyan A, Murukarthick J, Renganathan VG, Thangaraj K, Vellaikumar S, Vanniarajan C, Senthil N (2018) Genetic diversity in the barnyard millet (Echinochloa frumentacea) germplasms revealed by morphological traits and simple sequence repeat markers. Curr Plant Biol 14:71–78CrossRefGoogle Scholar
  24. Miah G, Rafii MY, Ismail MR, Puteh AB, Rahim HA, Islam KHN, Latif MA (2013) A review of microsatellite markers and their applications in rice breeding programs to improve blast disease resistance. Int J Mol Sci 14:22499–22528CrossRefGoogle Scholar
  25. Mondal TK, Ganie SA (2014) Identification and characterization of salt responsive miRNA-SSR markers in rice (Oryza sativa). Gene 535:204–209CrossRefGoogle Scholar
  26. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185CrossRefGoogle Scholar
  27. Muthamilarasan M, Dhaka A, Yadav R, Prasad M (2016) Exploration of millet models for developing nutrient rich graminaceous crops. Plant Sci 242:89–97CrossRefGoogle Scholar
  28. Nah G, Im JH, Kim JW, Park HR, Yook MJ, Yang TJ, Fischer AJ, Kim DS (2015) Uncovering the differential molecular basis of adaptive diversity in three Echinochloa leaf transcriptomes. PLoS One 10(8):e0134419CrossRefGoogle Scholar
  29. Nirmalakumari A, Subramanian A, Sumathi V, Senthil N, Kumaravadivel N, John A, Mohanasundaram K, Muthiah AR, Raveendran TS, Raguchander T, Manoharan S (2009) A high yielding kudiraivali variety CO (KV) 2. Madras Agric J 96:319–321Google Scholar
  30. Nishizawa NK (2005) The uptake and translocation of minerals in rice plants. In: Heong KL, Hardy B (eds) Toriyama K. IRRI, Philippines, pp 90–93Google Scholar
  31. Obidiegwu ON, Parzies H, Obidiegwu JE (2014) Development and genotyping potentials of EST-SSRs in finger millet (E. coracana (L.) Gaertn.). Int J Genet Genom 2:42–46CrossRefGoogle Scholar
  32. Osakabe Y, Osakabe K, Shinozaki K, Tran LSP (2014) Response of plants to water stress. Front Plant Sci 5:86CrossRefGoogle Scholar
  33. Pandey G, Misra G, Kumari K, Gupta S, Parida SK, Chattopadhyay D, Prasad M (2013) Genome-wide development and use of microsatellite markers for large-scale genotyping applications in foxtail millet [Setaria italica (L.)]. DNA Res 20:197–207CrossRefGoogle Scholar
  34. Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PloS One 7:e30619CrossRefGoogle Scholar
  35. Perumal S, Jayakodi M, Kim DS, Yang TJ, Natesan S (2016) The complete chloroplast genome sequence of Indian barnyard millet, Echinochloa frumentacea (Poaceae). Mitochondrial DNA Part B 1:79–80CrossRefGoogle Scholar
  36. Pfeiffer WH, McClafferty B (2007) HarvestPlus: breeding crops for better nutrition. Crop Sci 47:88–105CrossRefGoogle Scholar
  37. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140CrossRefGoogle Scholar
  38. Sood S, Khulbe RK, Gupta AK, Agrawal PK, Upadhyaya HD, Bhatt JC (2015) Barnyard millet—a potential food and feed crop of future. Plant Breed 134:135–147CrossRefGoogle Scholar
  39. Tadele Z (2016) Abiotic and biotic stress in plants—recent advances and future perspectives. In: AK Shanker, C Shanker (ed). InTech, London pp 768.Google Scholar
  40. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky JA (2006) NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314:1298–1301CrossRefGoogle Scholar
  41. Upadhyaya HD, Bajaj D, Das S, Kumar V, Gowda CLL, Sharma S, Tyagi AK, Parida SK (2016) Genetic dissection of seed-iron and zinc concentrations in chickpea. Sci Rep 6:20450CrossRefGoogle Scholar
  42. Varshney RK, Marcel TC, Ramsay L, Russell J, Röder MS, Stein N, Waugh R, Langridge P, Niks RE, Graner A (2007) A high density barley microsatellite consensus map with 775 SSR loci. Theor Appl Genet 114:1091–1103CrossRefGoogle Scholar
  43. Vatanparast M, Shetty P, Chopra R, Doyle JJ, Sathyanarayana N, Egan AN (2016) Transcriptome sequencing and marker development in winged bean (Psophocarpus tetragonolobus; Leguminosae). Sci Rep 6:29070CrossRefGoogle Scholar
  44. Veena B, Chimmad BV, Naik RK, Shantakumar G (2005) Physico-chemical and nutritional studies in barnyard millet. Karnataka J Agril Sci 18:101–105Google Scholar
  45. Wei W, Qi X, Wang L, Zhang Y, Hua W, Li D, Lv H, Zhang X (2011) Characterization of the sesame (Sesamum indicum L.) global transcriptome using Illumina paired-end sequencing and development of EST-SSR markers. BMC Genom 12:451CrossRefGoogle Scholar
  46. Xu H, Luo X, Qian J, Pang X, Song J, Qian G, Chen J, Chen S (2012) FastUniq: a fast de novo duplicates removal tool for paired short reads. PLoS One 7:e52249CrossRefGoogle Scholar
  47. Yamasue Y, Asai Y, Ueki K, Kusanagi T (1989) Anaerobic seed germination for the habitat segregation in Echinochloa weeds. Jpn J Breed 39:159–168CrossRefGoogle Scholar
  48. Yamasue Y, Nakamura A, Ueki K, Kusanagi T (1989) Drought resistance for the habitat segregation in Echinochloa weeds. Jpn J Breed 39:337–343CrossRefGoogle Scholar
  49. Yang X, Yu XY, Li YF (2013) De novo assembly and characterization of the barnyardgrass (Echinochloa crus-galli) transcriptome using next-generation pyrosequencing. PloS One 8:e69168CrossRefGoogle Scholar
  50. Yue R, Lu C, Qi J, Han X, Yan S, Guo S, Liu L, Fu X, Chen N, Yin H, Chi H, Tie S (2016) Transcriptome analysis of cadmium-treated roots in maize (Zea mays L.). Front Plant Sci 7:1298PubMedPubMedCentralGoogle Scholar
  51. Zhang J, Liang S, Duan J, Wang J, Chen S, Cheng Z, Zhang Q, Liang X, Li Y (2012) De novo assembly and characterisation of the transcriptome during seed development, and generation of genic-SSR markers in peanut (Arachis hypogaea L.). BMC Genom 13:90CrossRefGoogle Scholar
  52. Zhang S, Tang C, Zhao Q, Li J, Yang L, Qie L, Fan X, Li L, Zhang N, Zhao M, Liu X, Chai Y, Zhang X, Wang H, Li Y, Li W, Zhi H, Jia G, Diao X (2014) Development of highly polymorphic simple sequence repeat markers using genome-wide microsatellite variant analysis in Foxtail millet [Setaria italica (L.) P. Beauv.]. BMC Genom 15:78CrossRefGoogle Scholar
  53. Zhang ZF, Li YY, Xiao BZ (2016) Comparative transcriptome analysis highlights the crucial roles of photosynthetic system in drought stress adaptation in upland rice. Sci Rep 6:19349CrossRefGoogle Scholar
  54. Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang X, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  • Murukarthick Jayakodi
    • 1
  • Manimekalai Madheswaran
    • 2
  • Karthikeyan Adhimoolam
    • 3
  • Sampath Perumal
    • 4
  • Dhasarathan Manickam
    • 3
  • Thangaraj Kandasamy
    • 2
  • Tae-Jin Yang
    • 1
    Email author
  • Senthil Natesan
    • 3
    • 5
    Email author
  1. 1.Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute of Agriculture and Life Sciences, College of Agriculture and Life SciencesSeoul National UniversitySeoulRepublic of Korea
  2. 2.Department of Plant Breeding and Genetics, Agricultural College and Research InstituteTamil Nadu Agricultural UniversityMaduraiIndia
  3. 3.Department of Biotechnology, Agricultural College and Research InstituteTamil Nadu Agricultural UniversityMaduraiIndia
  4. 4.Agriculture and Agri-Food CanadaSaskatoonCanada
  5. 5.Department of Plant Molecular Biology and Bioinformatics, Centre for Plant Molecular Biology and BiotechnologyTamil Nadu Agricultural UniversityCoimbatoreIndia

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