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Unveiling gibberellin-responsive coding and long noncoding RNAs in maize

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We report coding and long noncoding RNAs in maize upon phytohormone gibberellin stimulation.

Abstract

Plant hormone gibberellin (GA) orchestrates various facets of biological processes. Dissection the transcriptomic dynamics upon GA stimulation has biological significance. Feature of maize transcriptome in response to GA application remains largely elusive. Herein, two types of plants, one was with normal height, the other was GA-sensitive dwarfism, were selected from advanced backcross population for GA3 treatment with different concentrations. In control and GA3-treated plants, we identified a large number of coding and long noncoding RNAs (lncRNAs) through sequencing eight ribosomal-depleted RNA libraries. Transcripts encoding GA biosynthetic and metabolic enzymes KS, GA20ox, GA3ox, and GA2ox were significantly differentially expressed in GA3-treated samples. A total of 78 protein-coding transcripts were shared between GA3-treated normal height and dwarf plants. Shared transcripts encoding terpene synthase, MYB transcription factor, and receptor-like protein kinase were co-regulated with their corresponding partners. Out of identified lncRNAs, 22 and 34 significantly differentially expressed lncRNAs were responsive to GA application in normal height and dwarf plants, respectively. Shared GA-responsive lncRNAs were found in GA3-treated normal height and dwarf plants. Some lncRNAs corresponded to precursors of known miRNA, such as zma-miR528a and zma-miR528b. Multiple promising targets of significantly differentially expressed lncRNAs were discovered, including Lazy plant1 for auxin- and GA-mediated shoot gravitropism, bZIP transcription factor member for GA-controlled cell elongation. This study will improve our knowledge of GA-triggered transcriptome change and facilitate a comprehensive understanding of regulatory cascade centering on GA.

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References

  • Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159

    Article  CAS  Google Scholar 

  • Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G (2004) GO::TermFinder-open source software for accessing gene ontology information and finding significantly enriched gene ontology terms associated with a list of genes. Bioinformatics 20:3710–3715

    Article  CAS  Google Scholar 

  • Brosnan CA, Voinnet O (2009) The long and the short of noncoding RNAs. Curr Opin Cell Biol 21:416–425

    Article  CAS  Google Scholar 

  • Chen X, Lu S, Wang Y, Zhang X, Lv B, Luo L, Xi D, Shen J, Ma H, Ming F (2015) OsNAC2 encoding a NAC transcription factor that affects plant height through mediating the gibberellic acid pathway in rice. Plant J 82:302–314

    Article  CAS  Google Scholar 

  • Dong Z, Jiang C, Chen X, Zhang T, Ding L, Song W, Luo H, Lai J, Chen H, Liu R, Zhang X, Jin W (2013) Maize LAZY1 mediates shoot gravitropism and inflorescence development through regulating auxin transport, auxin signaling, and light response. Plant Physiol 163:1306–1322

    Article  CAS  Google Scholar 

  • Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285

    Article  CAS  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037

    Article  CAS  Google Scholar 

  • Fukazawa J, Sakai T, Ishida S, Yamaguchi I, Kamiya Y, Takahashi Y (2000) Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell 12:901–915

    Article  CAS  Google Scholar 

  • Gene Ontology Consortium (2015) Gene ontology consortium: going forward. Nucleic Acids Res 43:D1049–D1056

    Article  Google Scholar 

  • Han J, Fang J, Wang C, Yin Y, Sun X, Leng X, Song C (2014) Grapevine microRNAs responsive to exogenous gibberellin. BMC Genomics 15:111

    Article  CAS  Google Scholar 

  • Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79

    Article  CAS  Google Scholar 

  • Jabnoune M, Secco D, Lecampion C, Robaglia C, Shu Q, Poirier Y (2013) A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness. Plant Cell 25:4166–4182

    Article  CAS  Google Scholar 

  • Jiang X, Li H, Wang T, Peng C, Wang H, Wu H, Wang X (2012) Gibberellin indirectly promotes chloroplast biogenesis as a means to maintain the chloroplast population of expanded cells. Plant J 72:768–780

    Article  CAS  Google Scholar 

  • Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45:D353–D361

    Article  CAS  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

    Article  Google Scholar 

  • Kim ED, Xiong Y, Pyo Y, Kim DH, Kang BH, Sung S (2017) Spatio-temporal analysis of coding and long noncoding transcripts during maize endosperm development. Sci Rep 7:3838

    Article  Google Scholar 

  • Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349

    Article  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73

    Article  CAS  Google Scholar 

  • Li L, Eichten SR, Shimizu R, Petsch K, Yeh CT, Wu W, Chettoor AM, Givan SA, Cole RA, Fowler JE, Evans MM, Scanlon MJ, Yu J, Schnable PS, Timmermans MC, Springer NM, Muehlbauer GJ (2014) Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biol 15:R40

    Article  Google Scholar 

  • Liu Y, Xu Y, Xiao J, Ma Q, Li D, Xue Z, Chong K (2011) OsDOG, a gibberellin-induced A20/AN1 zinc-finger protein, negatively regulates gibberellin-mediated cell elongation in rice. J Plant Physiol 168:1098–1105

    Article  CAS  Google Scholar 

  • Liu Q, Hu H, Zhu L, Li R, Feng Y, Zhang L, Yang Y, Liu X, Zhang H (2015) Involvement of miR528 in the regulation of arsenite tolerance in rice (Oryza sativa L.). J Agric Food Chem 63:8849–8861

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2011) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  Google Scholar 

  • Lv Y, Liang Z, Ge M, Qi W, Zhang T, Lin F, Peng Z, Zhao H (2016) Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize (Zea mays L.). BMC Genomics 17:350

    Article  Google Scholar 

  • Middleton AM, Úbeda-Tomás S, Griffiths J, Holman T, Hedden P, Thomas SG, Phillips AL, Holdsworth MJ, Bennett MJ, King JR, Owen MR (2012) Mathematical modeling elucidates the role of transcriptional feedback in gibberellin signaling. Proc Natl Acad Sci USA 109:7571–7576

    Article  CAS  Google Scholar 

  • Qin T, Zhao H, Cui P, Albesher N, Xiong L (2017) A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance. Plant Physiol 175:1321–1336

    Article  CAS  Google Scholar 

  • Rood SB, Kaufman PB, Abe H, Pharis RP (1987) Gibberellins and gravitropism in maize shoots: endogenous gibberellin-like substances and movement and metabolism of [3H]Gibberellin A20. Plant Physiol 83:645–651

    Article  CAS  Google Scholar 

  • Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802

    Article  CAS  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–D452

    Article  CAS  Google Scholar 

  • Tafer H, Hofacker IL (2008) RNAplex: a fast tool for RNA-RNA interaction search. Bioinformatics 24:2657–2663

    Article  CAS  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  Google Scholar 

  • Wang Y, Deng D (2014) Molecular basis and evolutionary pattern of GA-GID1-DELLA regulatory module. Mol Genet Genomics 289:1–9

    Article  CAS  Google Scholar 

  • Wang Y, Lu W, Chen Y, Deng D, Ding H, Bian Y, Yin Z, Zhu Y, Zhao J (2016a) Revealing physiological and genetic properties of a dominant maize dwarf Dwarf11 (D11) by integrative analysis. Mol Breed 36:31

    Article  Google Scholar 

  • Wang B, Tseng E, Regulski M, Clark TA, Hon T, Jiao Y, Lu Z, Olson A, Stein JC, Ware D (2016b) Unveiling the complexity of the maize transcriptome by single-molecule long-read sequencing. Nat Commun 7:11708

    Article  CAS  Google Scholar 

  • Wang Y, Zhao J, Lu W, Deng D (2017) Gibberellin in plant height control: old player, new story. Plant Cell Rep 36:391–398

    Article  CAS  Google Scholar 

  • Wen BQ, Xing MQ, Zhang H, Dai C, Xue HW (2011) Rice homeobox transcription factor HOX1a positively regulates gibberellin responses by directly suppressing EL1. J Integr Plant Biol 53:869–878

    Article  CAS  Google Scholar 

  • Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 23:2184–2195

    Article  CAS  Google Scholar 

  • Wu Y, Wei B, Liu H, Li T, Rayner S (2011) MiRPara: a SVM-based software tool for prediction of most probable microRNA coding regions in genome scale sequences. BMC Bioinf 12:107

    Article  CAS  Google Scholar 

  • Wu H, Yang L, Chen LL (2017a) The diversity of long noncoding RNAs and their generation. Trends Genet 33:540–552

    Article  CAS  Google Scholar 

  • Wu J, Yang R, Yang Z, Yao S, Zhao S, Wang Y, Li P, Song X, Jin L, Zhou T, Lan Y, Xie L, Zhou X, Chu C, Qi Y, Cao X, Li Y (2017b) ROS accumulation and antiviral defence control by microRNA528 in rice. Nat Plants 3:16203

    Article  CAS  Google Scholar 

  • Xu D, Cao H, Fang W, Pan J, Chen J, Zhang J, Shen W (2017) Linking hydrogen-enhanced rice aluminum tolerance with the reestablishment of GA/ABA balance and miRNA-modulated gene expression: a case study on germination. Ecotoxicol Environ Saf 145:303–312

    Article  CAS  Google Scholar 

  • Yazaki J, Shimatani Z, Hashimoto A, Nagata Y, Fujii F, Kojima K, Suzuki K, Taya T, Tonouchi M, Nelson C, Nakagawa A, Otomo Y, Murakami K, Matsubara K, Kawai J, Carninci P, Hayashizaki Y, Kikuchi S (2004) Transcriptional profiling of genes responsive to abscisic acid and gibberellin in rice: phenotyping and comparative analysis between rice and Arabidopsis. Physiol Genomics 17:87–100

    Article  CAS  Google Scholar 

  • Yoon JH, Abdelmohsen K, Gorospe M (2014) Functional interactions among microRNAs and long noncoding RNAs. Semin Cell Dev Biol 34:9–14

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31571671), the National Key Research and Development Program of China (2016YFD0101002), the Key Research Program of Jiangsu Provincial Colleges and Universities (18KJA210002), the Innovative Foundation of Yangzhou University (2017CXJ063), the Science Foundation for Excellent Youth Scholars of Yangzhou University, the Priority Academic Program Development of Jiangsu Higher Education Institutions, and the Practicality and Innovation Training Project for College Students of Yangzhou University (x20160631, x20170646).

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Authors

Contributions

YJW conceived and designed the experiments. DD prepared the experimental materials. YLW, JZ, JH, and YS performed the experiments. YJW and YLW analyzed the data. YJW wrote the manuscript.

Corresponding author

Correspondence to Yijun Wang.

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The authors declare that they have no conflict of interest.

Electronic supplementary material

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11103_2018_788_MOESM1_ESM.png

Fig. S1 Structure of miRNA precursor. Significantly differentially expressed lncRNA TCONS_00051916 could be the miRNA precursor (PNG 17 KB)

Fig. S2 Antisense target of significantly differentially expressed lncRNA TCONS_00110864 (PNG 118 KB)

Fig. S3 Interaction network of target genes of significantly differentially expressed lncRNAs (TIF 243 KB)

Table S1

Primers used in this study (DOCX 14 KB)

Table S2 Information of significantly differentially expressed protein-coding transcripts (XLSX 91 KB)

11103_2018_788_MOESM6_ESM.xlsx

Table S3 Gene ontology enrichment analysis of significantly differentially expressed protein-coding transcripts (XLSX 11 KB)

Table S4 Functional annotation of shared GA-responsive protein-coding transcripts (XLSX 13 KB)

Table S5 Information of all identified lncRNAs and shared GA-responsive lncRNAs (XLSX 679 KB)

Table S6 Information of significantly differentially expressed lncRNAs (XLSX 15 KB)

Table S7 GA-responsive lncRNAs as precursors of miRNAs (XLSX 16 KB)

Table S8 Cis targets of significantly differentially expressed lncRNAs in D11 upon GA3 application (XLSX 10 KB)

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Wang, Y., Wang, Y., Zhao, J. et al. Unveiling gibberellin-responsive coding and long noncoding RNAs in maize. Plant Mol Biol 98, 427–438 (2018). https://doi.org/10.1007/s11103-018-0788-8

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