Abstract
Drought is a major abiotic stress affecting crop productivity and quality. As a class of noncoding RNA, microRNA (miRNA) plays important roles in plant growth, development, and stress response. However, their response and roles in tomato drought stress is largely unknown. Here, by using high-throughput sequencing, we compared the miRNA profiles before and after drought treatment in two tomato genotypes: M82, a drought-sensitive cultivated tomato (Solanum lycopersicum), and IL2-5, a drought-tolerant introgression line derived from M82 and the tomato wild species S. pennellii (LA0716). A total of 108 conserved and 208 novel miRNAs were identified, among them, 32 and 68 were significantly changed in expression after stress. Further, 1936 putative target genes were predicted for those differentially-expressed miRNAs. Gene ontology and pathway analysis showed that many of the target genes were involved in stress resistance, such as genes in GO terms including response to stress, defense response, response to stimulus, phosphorylation, and signal transduction. Our results suggested that miRNAs play an essential role in the drought response of tomato. This work will help to further characterize specific miRNAs functioning in drought tolerance.
Similar content being viewed by others
Abbreviations
- miRNA:
-
microRNA
- nt:
-
Nucleotide
- qRT-PCR:
-
Quantitative real-time PCR
- GO:
-
Gene ontology
- KEGG:
-
Kyoto encyclopedia of genes and genomes
References
Alptekin B, Langridge P, Budak H (2017) Abiotic stress miRNomes in the Triticeae. Funct Integr Genomics 17:145–170
Alseekh S, Ofner I, Pleban T, Tripodi P, Dato FD, Cammareri M, Mohammad A, Grandillo S, Fernie AR, Zamir D (2013) Resolution by recombination: breaking up Solanum pennellii introgressions. Trends Plant Sci 18:536–538
Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Bolger A, Scossa F, Bolger ME et al (2014) The genome of the stress-tolerant wild tomato species Solanum pennellii. Nat Genet 46:1034–1038
Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genomics 15:523–531
Budak H, Kantar M, Bulut R, Akpinar BA (2015) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13
Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A (2013) Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41:226–232
Candar-Cakir B, Arican E, Zhang B (2016) Small RNA and degradome deep sequencing reveals drought-and tissue-specific micrornas and their important roles in drought-sensitive and drought-tolerant tomato genotypes. Plant Biotechnol J 14:1727–1746
Cao X, Wu Z, Jiang F, Zhou R, Yang Z (2014) Identification of chilling stress-responsive tomato microRNAs and their target genes by high-throughput sequencing and degradome analysis. BMC Genomics 15:1130
Capel C, Fernandez del Carmen A, Alba JM, Lima-Silva V, Hernandez-Gras F, Salinas M, Boronat A, Angosto T, Botella MA, Fernandez-Munoz R, Granell A, Capel J, Lozano R (2015) Wide-genome QTL mapping of fruit quality traits in a tomato RIL population derived from the wild-relative species Solanum pimpinellifolium L. Theor Appl Genet 128:2019–2035
Cheah BH, Nadarajah K, Divate MD, Wickneswari R (2015) Identification of four functionally important microRNA families with contrasting differential expression profiles between drought-tolerant and susceptible rice leaf at vegetative stage. BMC Genomics 16:692
Chuck G, Candela H, Hake S (2009) Big impacts by small RNAs in plant development. Curr Opin Plant Biol 12:81–86
The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2014) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 80:1108–1117
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159
Ding Y, Tao Y, Zhu C (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J Exp Bot 64:3077–3086
Eshed Y, Zamir D (1994) A genomic library of Lycopersicon pennellii in L. esculentum: A tool for fine mapping of genes. Euphytica 79:175–179
Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219
Ferdous J, Hussain SS, Shi BJ (2015) Role of microRNAs in plant drought tolerance. Plant Biotechnol J 13:293–305
Gallie DR (2013) The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot 64:433–443
Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2+ signalling to membrane dynamics. Nat Rev Mol Cell Biol 6:449–461
Gong P, Zhang J, Li H, Yang C, Zhang C, Zhang X, Khurram Z, Zhang Y, Wang T, Fei Z, Ye Z (2010) Transcriptional profiles of drought-responsive genes in modulating transcription signal transduction, and biochemical pathways in tomato. J Exp Bot 61:3563–3575
Griffiths-Jones S, Saini HK, Van DS, Enright AJ (2008) MiRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154–D158
Ilahy R, Piro G, Tlili I, Riahi A, Sihem R, Ouerghi I, Hdider C, Lenucci MS (2016) Fractionate analysis of the phytochemical composition and antioxidant activities in advanced breeding lines of high-lycopene tomatoes. Food Funct 7:574–583
Iovieno P, Punzo P, Guida G, Mistretta C, Van Oosten MJ, Nurcato R, Bostan H, Colantuono C, Costa A, Bagnaresi P, Chiusano ML, Albrizio R, Giorio P, Batelli G, Grillo S (2016) Transcriptomic changes drive physiological responses to progressive drought stress and rehydration in tomato. Front Plant Sci 7:371
Ivits E, Horion S, Fensholt R, Cherlet M (2014) Drought footprint on European ecosystems between 1999 and 2010 assessed by remotely sensed vegetation phenology and productivity. Globe Change Biol 20:581–593
Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207
Jin W, Wu F (2015) Characterization of miRNAs associated with Botrytis cinerea infection of tomato leaves. BMC Plant Biol 15:1
Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045
Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M (2014) Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 42:D199–D205
Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genomics 10:493–507
Karlova R, van Haarst JC, Maliepaard C, van de Geest H, Bovy AG, Lammers M, Angenent GC, de Maagd RA (2013) Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. J Exp Bot 64:1863–1878
Kidner CA, Martienssen RA (2005) The developmental role of microRNA in plants. Curr Opin Plant Biol 8:38–44
Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59
Konopka-Postupolska D, Clark G, Goch G, Debski J, Floras K, Cantero A, Fijolek B, Roux S, Hennig J (2009) The role of annexin 1 in drought stress in Arabidopsis. Plant Physiol 150:1394–1410
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Laohavisit A, Davies JM (2011) Annexins. New Phytol 189:40–53
Lawlor DW (2013) Genetic engineering to improve plant performance under drought: physiological evaluation of achievements, limitations, and possibilities. J Exp Bot 64:83–108
Lei J, Sun Y (2014) MiR-PREFeR: an accurate, fast and easy-to-use plant miRNA prediction tool using small RNA-Seq data. Bioinformatics 30:2837–2839
Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251
Lin T, Zhu G, Zhang J, Xu X, Yu Q, Zheng Z, Zhang Z, Lun Y, Li S, Wang X (2014) Genomic analyses provide insights into the history of tomato breeding. Nat Genet 46:1220–1226
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843
Liu H, Searle IR, Watson-Haigh NS, Baumann U, Mather DE, Able AJ, Able JA (2015) Genome-wide identification of microRNAs in leaves and the developing head of four durum genotypes during water deficit stress. PLoS One 10:e0142799
Liu H, Able AJ, Able JA (2016) SMARTER de-stressed cereal breeding. Trends Plant Sci 21:909–925
Liu M, Yu H, Zhao G, Huang Q, Lu Y, Ouyang B (2017) Profiling of drought-responsive microRNA and mRNA in tomato using high-throughput sequencing. BMC Genomics 18:481
Lu Y, Ouyang B, Zhang J, Wang T, Lu C, Han Q, Zhao S, Ye Z, Li H (2012) Genomic organization, phylogenetic comparison and expression profiles of annexin gene family in tomato (Solanum lycopersicum). Gene 499:14–24
Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, Davies JM (2008) Annexins: multifunctional components of growth and adaptation. J Exp Bot 59:533–544
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295
Pradhan B, Naqvi AR, Saraf S, Mukherjee SK, Dey N (2015) Prediction and characterization of Tomato leaf curl New Delhi virus (ToLCNDV) responsive novel microRNAs in Solanum lycopersicum. Virus Res 195:183–195
Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425
Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108
Seneviratne SI (2012) Climate science: historical drought trends revisited. Nature 491:338–339
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
Shirasawa K, Isobe S, Hirakawa H, Asamizu E, Fukuoka H, Just D, Rothan C, Sasamoto S, Fujishiro T, Kishida Y, Kohara M, Tsuruoka H, Wada T, Nakamura Y, Sato S, Tabata S (2010) SNP discovery and linkage map construction in cultivated tomato. DNA Res 17:381–391
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203
Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195
Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367
Wei L, Zhang D, Xiang F, Zhang Z (2009) Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. Int J Plant Sci 170:979–989
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210
Xie F, Wang Q, Sun R, Zhang B (2015a) Deep sequencing reveals important roles of microRNAs in response to drought and salinity stress in cotton. J Exp Bot 66:789–804
Xie M, Zhang S, Yu B (2015b) MicroRNA biogenesis, degradation and activity in plants. Cell Mol Life Sci 72:87–99
Xu J, Yuan Y, Xu Y, Zhang G, Guo X, Wu F, Wang Q, Rong T, Pan G, Cao M, Tang Q, Gao S, Liu Y, Wang J, Lan H, Lu Y (2014) Identification of candidate genes for drought tolerance by whole-genome resequencing in maize. BMC Plant Biol 14:83
Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.) Genome Biol 8:R96
Zhang B (2015) MicroRNA: a new target for improving plant tolerance to abiotic stress. J Exp Bot 66:1749–1761
Zhang F, Li S, Yang S, Wang L, Guo W (2015) Overexpression of a cotton annexin gene, GhAnn1, enhances drought and salt stress tolerance in transgenic cotton. Plant Mol Biol 87:47–67
Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590
Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 1779:780–788
Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168
Zhu X, Xiong L (2013) Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced wax deposition in rice. PNAS 110:17790–17795
Zhuang J, Zhang J, Hou XL, Wang F, Xiong AS (2014) Transcriptomic, proteomic, metabolomic and functional genomic approaches for the study of abiotic stress in vegetable crops. Crit Rev Plant Sci 33:225–237
Funding
This work was supported by the National Natural Science Foundation of China (U1503186, 31572133) and the Applied Basic Research Program (2016020101010092) of Science and Technology Bureau of Wuhan City, Hubei, China.
Author information
Authors and Affiliations
Contributions
Bo Ouyang and Minmin Liu designed the experiments and wrote the manuscript. Minmin Liu and Huiyang Yu analyzed the data. Minmin Liu, Gangjun Zhao, Qiufeng Huang, and Yongen Lu carried out the experiments. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Supplementary Table S1
- Conserved miRNAs expressed in the drought-sensitive and -tolerant tomato genotypes. (XLSX 27 kb)
Supplementary Table S2
- Novel miRNAs expressed in drought-sensitive and -tolerant tomato genotypes. (XLSX 37 kb)
Supplementary Table S3
- Target gene prediction results of differentially-expressed miRNAs. (XLSX 456 kb)
Supplementary Table S4
- Enriched GO terms of drought-responsive miRNA targets in tomato. (XLSX 90 kb)
Supplementary Table S5
- KEGG pathway terms of drought-responsive miRNA targets in tomato. (XLSX 15 kb)
Supplementary Table S6
- The primers of miRNAs and target genes used for qRT-PCR verification. (XLSX 9 kb)
Rights and permissions
About this article
Cite this article
Liu, M., Yu, H., Zhao, G. et al. Identification of drought-responsive microRNAs in tomato using high-throughput sequencing. Funct Integr Genomics 18, 67–78 (2018). https://doi.org/10.1007/s10142-017-0575-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-017-0575-7