Plant Biotechnology Reports

, Volume 9, Issue 5, pp 279–286 | Cite as

Genome-wide screening for novel, drought stress-responsive long non-coding RNAs in drought-stressed leaf transcriptome of drought-tolerant and -susceptible banana (Musa spp) cultivars using Illumina high-throughput sequencing

  • M. Muthusamy
  • S. Uma
  • S. Backiyarani
  • M. S. Saraswathi
Original Article

Abstract

Long non-coding RNAs (LncRNAs) are one of the many layers of transcription in higher plants. LncRNAs are responsive to biotic and abiotic stresses and regulate genes. In our study, we have identified 905 novel lncRNAs from 8471 drought-responsive, novel transcripts of RNA-Seq reads from two banana cultivars, a drought-tolerant cv. ‘Saba’ (ABB) and -susceptible cv. ‘Grand Naine’ (AAA). Of these 905 lncRNAs, 75 (8.3 %) transcripts were natural antisense RNAs (NATs) and 2 transcripts identified as precursors of microRNA-miR156 and miR166. Among the 905 identified lncRNAs, 216, 150 and 279, 164 lncRNAs were induced and reduced to drought stress, respectively, in tolerant and susceptible in comparison to their equivalent controls. The remaining 22 lncRNA of tolerant cultivars was not regulated by drought stress. Of the 882 drought-responsive lncRNAs, 44 new lncRNAs were identified as induced. Musa lncRNAs were unevenly distributed in 11 chromosomes of Musa acuminata and no lncRNAs were found in chromosome-9 of drought-tolerant cultivar. The average lengths of lncRNAs were 683 nucleotides (nt). Drought-responsive differential expression of lncRNAs was found between +8.11585- and −4.04311-fold. Around 7.9 % of the identified lncRNAs were decoys of 85 conserved microRNAs. These findings will lay a basic platform for effective strategic planning of developing drought-resilient crop varieties.

Keywords

Banana lncRNA Drought stress-responsive lncRNA Natural antisense RNAs microRNA decoys Genome-wide screening for novel lncRNA 

Supplementary material

11816_2015_363_MOESM1_ESM.txt (646 kb)
Supplementary data. 1 A total of 905 predicted banana long non-coding RNA sequences (TXT 646 kb)
11816_2015_363_MOESM2_ESM.xlsx (136 kb)
Supplementary data. 2 Musa drought-responsive, novel lncRNA expression and coding potential from RNA-Seq data (XLSX 136 kb)
11816_2015_363_MOESM3_ESM.xlsx (35 kb)
Supplementary data. 3 Banana lncRNAs predicted as Natural Antisense RNAs (XLSX 35 kb)
11816_2015_363_MOESM4_ESM.xlsx (131 kb)
Supplementary data. 4 Banana LncRNAs predicted as microRNA target mimics (XLSX 130 kb)

References

  1. Amor BB, Wirth S, Merchan F et al (2009) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19:57–69. doi:10.1101/gr.080275.108.1 PubMedCentralCrossRefPubMedGoogle Scholar
  2. Boerner S, McGinnis KM (2012) Computational identification and functional predictions of long noncoding RNA in Zea mays. PLoS One 7:e43047. doi:10.1371/journal.pone.0043047 PubMedCentralCrossRefPubMedGoogle Scholar
  3. Chen D, Yuan C, Zhang J et al (2012) PlantNATsDB: a comprehensive database of plant natural antisense transcripts. Nucleic Acid Res 40:D1187–D1193. doi:10.1093/nar/gkr823 PubMedCentralCrossRefPubMedGoogle Scholar
  4. D’Hont A, Denoeud F, Aury J et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488(7410):213–217. doi:10.1038/nature11241 CrossRefPubMedGoogle Scholar
  5. Foissac S, Sammeth M (2007) ASTALAVISTA: dynamic and flexible analysis of alternative splicing events in custom gene datasets. Nucleic Acid Res 35:W297–W299. doi:10.1093/nar/gkm311 PubMedCentralCrossRefPubMedGoogle Scholar
  6. Griffiths-Jones S (2003) Rfam: an RNA family database. Nucleic Acid Res 31:439–441. doi:10.1093/nar/gkg006 PubMedCentralCrossRefPubMedGoogle Scholar
  7. Hao Z, Fan C, Cheng T et al (2015) Genome-wide identification, characterization and evolutionary analysis of long intergenic noncoding RNAs in cucumber. PLoS One 10:e0121800. doi:10.1371/journal.pone.0121800 PubMedCentralCrossRefPubMedGoogle Scholar
  8. Henz SR, Cumbie JS, Kasschau KD et al (2007) Distinct expression patterns of natural antisense transcripts in Arabidopsis. Plant Physiol 144:1247–1255. doi:10.1104/pp.107.100396 PubMedCentralCrossRefPubMedGoogle Scholar
  9. Kalyna M, Simpson CG, Syed NH et al (2012) Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acid Res 40:2454–2469. doi:10.1093/nar/gkr932 PubMedCentralCrossRefPubMedGoogle Scholar
  10. Kong L, Zhang Y, Ye ZQ et al (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acid Res 35:W345–W349. doi:10.1093/nar/gkm391 PubMedCentralCrossRefPubMedGoogle Scholar
  11. Kornienko AE, Guenzl PM, Barlow DP, Pauler FM (2013) Gene regulation by the act of long non-coding RNA transcription. BMC Biol 11:59. doi:10.1186/1741-7007-11-59 PubMedCentralCrossRefPubMedGoogle Scholar
  12. Liu J, Jung C, Xu J et al (2012) Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24:4333–4345. doi:10.1105/tpc.112.102855 PubMedCentralCrossRefPubMedGoogle Scholar
  13. Meng Y, Shao C, Wang H, Jin Y (2012) Target mimics: an embedded layer of microRNA-involved gene regulatory networks in plants. BMC Genomic 13:197. doi:10.1186/1471-2164-13-197 CrossRefGoogle Scholar
  14. Min XJ (2013) ASFinder: a tool for genome-wide identification of alternatively splicing transcripts from EST-derived sequences. Int J Bioinform Res Appl 9:221–226. doi:10.1504/IJBRA.2013.053603 CrossRefPubMedGoogle Scholar
  15. Muthusamy M, Uma S, Backiyarani S, Saraswathi MS et al (2014) Computational prediction, identification, and expression profiling of microRNAs in banana. J Hortic Sci Biotech 89:208–214Google Scholar
  16. Osato N, Suzuki Y, Ikeo K, Gojobori T (2007) Transcriptional interferences in cis natural antisense transcripts of humans and mice. Genetics 176:1299–1306. doi:10.1534/genetics.106.069484 PubMedCentralCrossRefPubMedGoogle Scholar
  17. Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136:629–641. doi:10.1016/j.cell.2009.02.006 CrossRefPubMedGoogle Scholar
  18. Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acid Res 33:W686–W689. doi:10.1093/nar/gki366 PubMedCentralCrossRefPubMedGoogle Scholar
  19. Shinozaki K, Yamaguchi-shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227. doi:10.1093/jxb/erl164 CrossRefPubMedGoogle Scholar
  20. Shuai P, Liang D, Tang S et al (2014) Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. J Exp Bot 65:4975–4983. doi:10.1093/jxb/eru256 PubMedCentralCrossRefPubMedGoogle Scholar
  21. Sun L, Zhang Z, Bailey TL et al (2012) Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. BMC Bioinform 13:331. doi:10.1186/1471-2105-13-331 CrossRefGoogle Scholar
  22. Surendar KK, Devi DD, Ravi I et al (2013) Water Stress in Banana—a Review. Bull Env Pharmacol Life Sci 2:1–18Google Scholar
  23. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111. doi:10.1093/bioinformatics/btp120 PubMedCentralCrossRefPubMedGoogle Scholar
  24. Van Asten PJA, Fermont AM, Taulya G (2010) Drought is a major yield loss factor for rainfed East African highland banana. Agric Water Manag 98:541–552. doi:10.1016/j.agwat.2010.10.005 CrossRefGoogle Scholar
  25. Wang XJ, Gaasterland T, Chua NH (2005) Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol 6:R30. doi:10.1186/gb-2005-6-4-r30 PubMedCentralCrossRefPubMedGoogle Scholar
  26. Wang H, Chung PJ, Liu J et al (2014) Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24:444–453. doi:10.1101/gr.165555.113.2006 PubMedCentralCrossRefPubMedGoogle Scholar
  27. Wu HJ, Ma YK, Chen T et al (2012) PsRobot: a web-based plant small RNA meta-analysis toolbox. Nucleic Acid Res 40:W22–W28. doi:10.1093/nar/gks554 PubMedCentralCrossRefPubMedGoogle Scholar
  28. Wu HJ, Wang ZM, Wang M, Wang XJ (2013) Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol 161:1875–1884. doi:10.1104/pp.113.215962 PubMedCentralCrossRefPubMedGoogle Scholar
  29. Xin M, Wang Y, Yao Y et al (2011) Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol 11:61. doi:10.1186/1471-2229-11-61 PubMedCentralCrossRefPubMedGoogle Scholar
  30. Yi X, Zhang Z, Ling Y et al (2015) PNRD: a plant non-coding RNA database. Nucleic Acid Res 43:D982–D989. doi:10.1093/nar/gku1162 PubMedCentralCrossRefPubMedGoogle Scholar
  31. Zhang X, Xia J, Lii YE et al (2012) Genome-wide analysis of plant nat-siRNAs reveals insights into their distribution, biogenesis and function. Genome Biol 13:R20. doi:10.1186/gb-2012-13-3-r20 PubMedCentralCrossRefPubMedGoogle Scholar
  32. Zhang J, Mujahid H, Hou Y et al (2013) Plant long ncRNAs: a new frontier for gene regulatory control. Am J Plant Sci 04:1038–1045. doi:10.4236/ajps.2013.45128 CrossRefGoogle Scholar
  33. Zhang YC, Liao JY, Li ZY et al (2014) Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol 15:512. doi:10.1186/s13059-014-0512-1 PubMedCentralCrossRefPubMedGoogle Scholar
  34. Zheng H, Qiyan J, Zhiyong N, Hui Z (2013) Prediction and identification of natural antisense transcripts and their small RNAs in soybean (Glycine max). BMC Genomic 14:280. doi:10.1186/1471-2164-14-280 CrossRefGoogle Scholar
  35. Zhu QH, Wang MB (2012) Molecular functions of long non-coding RNAs in plants. Genes (Basel) 3:176–190. doi:10.3390/genes3010176 CrossRefGoogle Scholar
  36. Zivkovic S, Popovic M, Dragisic-Maksimovic J et al (2010) Dehydration-related changes of peroxidase and polyphenol oxidase activity in fronds of the resurrection fern Asplenium ceterach L. Arch Biol Sci 62:1071–1081. doi:10.2298/ABS1004071Z CrossRefGoogle Scholar

Copyright information

© Korean Society for Plant Biotechnology and Springer Japan 2015

Authors and Affiliations

  1. 1.ICAR-National Research Centre for BananaTiruchirapalliIndia

Personalised recommendations