Skip to main content

Advertisement

SpringerLink
Log in

Small open reading frames in plant research: from prediction to functional characterization

  • Review Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Gene prediction is a laborious and time-consuming task. The advancement of sequencing technologies and bioinformatics tools, coupled with accelerated rate of ribosome profiling and mass spectrometry development, have made identification of small open reading frames (sORFs) (< 100 codons) in various plant genomes possible. The past 50 years have seen sORFs being isolated from many organisms. However, to date, a comprehensive sORF annotation pipeline is as yet unavailable, hence, addressed in our review. Here, we also provide current information on classification and functions of plant sORFs and their potential applications in crop improvement programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Availability of data and materials

Not applicable.

Code availability

Not applicable.

References

  • Abe K, Ichikawa H (2016) Gene overexpression resources in cereals for functional genomics and discovery of useful genes. Front Plant Sci 7:1359

    Article  PubMed  PubMed Central  Google Scholar 

  • Adams MD, Kelley JM, Gocayne JD, Dubnick M, Polymeropoulos MH, Xiao H et al (1991) Complementary DNA sequencing: expressed sequence tags and human genome project. Science 252(5013):1651–1656

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson DM, Anderson KM, Chang CL, Makarewich CA, NelsonMcAnally BR et al (2015) A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 160(4):595–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews SJ, Rothnagel JA (2014) Emerging evidence for functional peptides encoded by short open reading frames. Nat Rev Genet 15(3):193–204

    Article  CAS  PubMed  Google Scholar 

  • Aspden JL, Eyre-Walker YC, Phillips RJ, Amin U, Mumtaz MAS, Brocard M, Couso JP (2014) Extensive translation of small open reading frames revealed by Poly-Ribo-Seq. Elife 3(e03528):88

    Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297

    Article  CAS  PubMed  Google Scholar 

  • Bashir K, Hanada K, Shimizu M, Seki M, Nakanishi H, Nishizawa NK (2014) Transcriptomic analysis of rice in response to iron deficiency and excess. Rice 7(1):18

    Article  PubMed  PubMed Central  Google Scholar 

  • Basrai MA, Hieter P, Boeke JD (1997) Small open reading frames: beautiful needles in the haystack. Genome Res 7(8):768–771

    Article  CAS  PubMed  Google Scholar 

  • Bazin J, Baerenfaller K, Gosai SJ, Gregory BD, Crespi M, Bailey-Serres J (2017) Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation. Proc Natl Acad Sci 114(46):E10018–E10027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bazzini AA, Johnstone TG, Christiano R, Mackowiak SD, Obermayer B, Fleming ES et al (2014) Identification of small ORF s in vertebrates using ribosome footprinting and evolutionary conservation. EMBO J 33(9):981–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatta A, Atianand M, Jiang Z, Crabtree J, Blin J, Fitzgerald KA (2020) A Mitochondrial micropeptide is required for activation of the Nlrp3 inflammasome. J Immunol 204(2):428–437

    Article  CAS  PubMed  Google Scholar 

  • Blanvillain R, Young B, Cai YM, Hecht V, Varoquaux F, Delorme V et al (2011) The Arabidopsis peptide kiss of death is an inducer of programmed cell death. EMBO J 30(6):1173–1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blevins WR, Tavella T, Moro SG, Blasco-Moreno B, Closa-Mosquera A, Díez J et al (2019) Extensive post-transcriptional buffering of gene expression in the response to severe oxidative stress in baker’s yeast. Sci Rep 9(1):1–11

    Article  CAS  Google Scholar 

  • Bonneau L, Ge Y, Drury GE, Gallois P (2008) What happened to plant caspases? J Exp Bot 59(3):491–499

    Article  CAS  PubMed  Google Scholar 

  • Bontinck M, Van Leene J, Gadeyne A, De Rybel B, Eeckhout D, Nelissen H, De Jaeger G (2018) Recent trends in plant protein complex analysis in a developmental context. Front Plant Sci 9:640

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouché N, Bouchez D (2001) Arabidopsis gene knockout: phenotypes wanted. Curr Opinion Plant Biol 4(2):111–117

    Article  Google Scholar 

  • Brown TA (2002) Sequencing genomes. In Genomes. 2nd edition: Wiley-Liss

  • Cabrera-Quio LE, Herberg S, Pauli A (2016) Decoding sORF translation–from small proteins to gene regulation. RNA Bio 13(11):1051–1059

    Article  Google Scholar 

  • Calviello L, Ohler U (2017) Beyond read-counts: Ribo-seq data analysis to understand the functions of the transcriptome. Trends Genet 33(10):728–744

    Article  CAS  PubMed  Google Scholar 

  • Calviello L, Mukherjee N, Wyler E, Zauber H, Hirsekorn A, Selbach M et al (2016) Detecting actively translated open reading frames in ribosome profiling data. Nat Methods 13(2):165–170

    Article  CAS  PubMed  Google Scholar 

  • Campalans A, Kondorosi A, Crespi M (2004) Enod40, a short open reading frame–containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 16(4):1047–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caschera F, Karim AS, Gazzola G, d’Aquino AE, Packard NH, Jewett MC (2018) High-throughput optimization cycle of a cell-free ribosome assembly and protein synthesis system. ACS Synthetic Biol 7(12):2841–2853

    Article  CAS  Google Scholar 

  • Cassidy L, Helbig AO, Kaulich PT, Weidenbach K, Schmitz RA, Tholey A (2020) Multidimensional separation schemes enhance the identification and molecular characterization of low molecular weight proteomes and short open reading frame-encoded peptides in top-down proteomics. J Proteom 230:103988

    Article  Google Scholar 

  • Casson SA, Chilley PM, Topping JF, Evans IM, Souter MA, Lindsey K (2002) The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell 14(8):1705–1721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng H, Soon Chan W, Li Z, Wang D, Liu S, Zhou Y (2011) Small open reading frames: current prediction techniques and future prospect. Curr Protein Pept Sci 12(6):503–507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chew GL, Pauli A, Rinn JL, Regev A, Schier AF, Valen E (2013) Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs. Development 140(13):2828–2834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu Q, Ma J, Saghatelian A (2015) Identification and characterization of sORF-encoded polypeptides. Crit Rev Biochem Mol Biol 50(2):134–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chugunova A, Navalayeu T, Dontsova O, Sergiev P (2018) Mining for small translated ORFs. J Proteome Res 17(1):1–11

    Article  CAS  PubMed  Google Scholar 

  • Chun SY, Rodriguez CM, Todd PK, Mills RE (2016) SPECtre: a spectral coherence-based classifier of actively translated transcripts from ribosome profiling sequence data. BMC Bioinform 17(1):1–6

    Article  Google Scholar 

  • Couso JP, Patraquim P (2017) Classification and function of small open reading frames. Nat Rev Mol Cell Biol 18(9):575–589

    Article  CAS  PubMed  Google Scholar 

  • Couzigou JM, Lauressergues D, Bécard G, Combier JP (2015) miRNA-encoded peptides (miPEPs): a new tool to analyze the roles of miRNAs in plant biology. RNA Bio 12(11):1178–1180

    Article  Google Scholar 

  • Davey RA, MacLean HE (2006) Current and future approaches using genetically modified mice in endocrine research. Am J Physiol Endocrinol Metab 291(3):E429–E438

    Article  CAS  PubMed  Google Scholar 

  • De Coninck B, Carron D, Tavormina P, Willem L, Craik DJ, Vos C et al (2013) Mining the genome of Arabidopsis thaliana as a basis for the identification of novel bioactive peptides involved in oxidative stress tolerance. J Exp Bot 64(17):5297–5307

    Article  PubMed  Google Scholar 

  • Djakovic S, Dyachok J, Burke M, Frank MJ, Smith LG (2006) BRICK1/HSPC300 functions with SCAR and the ARP2/3 complex to regulate epidermal cell shape in Arabidopsis. Development 133(6):1091–1100

    Article  CAS  PubMed  Google Scholar 

  • Dong X, Wang D, Liu P, Li C, Zhao Q, Zhu D, Yu J (2013) Zm908p11, encoded by a short open reading frame (sORF) gene, functions in pollen tube growth as a profilin ligand in maize. J Exp Bot 64(8):2359–2372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erhard F, Halenius A, Zimmermann C, L’Hernault A, Kowalewski DJ, Weekes MP et al (2018) Improved Ribo-seq enables identification of cryptic translation events. Nat Methods 15(5):363–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faure E, Delaye L, Tribolo S, Levasseur A, Seligmann H, Barthélémy RM (2011) Probable presence of an ubiquitous cryptic mitochondrial gene on the antisense strand of the cytochrome oxidase I gene. Biol Direct 6(1):1–22

    Article  Google Scholar 

  • Fesenko I, Kirov I, Kniazev A, Khazigaleeva R, Lazarev V, Kharlampieva D et al (2019) Distinct types of short open reading frames are translated in plant cells. Genome Res 29(9):1464–1477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fields AP, Rodriguez EH, Jovanovic M, Stern-Ginossar N, Haas BJ, Mertins P et al (2015) A regression-based analysis of ribosome-profiling data reveals a conserved complexity to mammalian translation. Mol Cell 60(5):816–827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fiume E, Fletcher JC (2012) Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 24(3):1000–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank MJ, Smith LG (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Bio 12(10):849–853

    Article  CAS  Google Scholar 

  • Fukuda H (2016) Signaling, transcriptional regulation, and asynchronous pattern formation governing plant xylem development. P Jpn Acad B 92(3):98–107

    Article  CAS  Google Scholar 

  • Galindo MI, Pueyo JI, Fouix S, Bishop SA, Couso JP (2007) Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol 5(5):e106

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao H, Qin Y, Guo R, Wu Y, Qiu D, Fu Y (2018) Enhanced plant growth promoting role of mPEG-PLGA-based nanoparticles as an activator protein PeaT1 carrier in wheat (Triticum aestivum L.). J Chem Technol Biotechnol 93(11):3143–3151

    Article  CAS  Google Scholar 

  • Goytain A, Ng T (2020) NanoString nCounter technology: high-throughput RNA validation. Chimeric RNA. Springer, New York, pp 125–139

    Chapter  Google Scholar 

  • Green T, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175(4023):776–777

    Article  CAS  PubMed  Google Scholar 

  • Guillén G, Díaz-Camino C, Loyola-Torres CA, Aparicio-Fabre R, Hernández-López A, Díaz-Sánchez M, Sanchez F (2013) Detailed analysis of putative genes encoding small proteins in legume genomes. Front Plant Sci 4:208

    Article  PubMed  PubMed Central  Google Scholar 

  • Guttman M, Russell P, Ingolia NT, Weissman JS, Lander ES (2013) Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154(1):240–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J et al (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Hammerling MJ, Krüger A, Jewett MC (2020) Strategies for in vitro engineering of the translation machinery. Nucleic Acids Res 48(3):1068–1083

    Article  CAS  PubMed  Google Scholar 

  • Hanada K, Zhang X, Borevitz JO, Li WH, Shiu SH (2007) A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res 17(5):632–640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanada K, Akiyama K, Sakurai T, Toyoda T, Shinozaki K, Shiu SH (2010) sORF finder: a program package to identify small open reading frames with high coding potential. Bioinformatics 26(3):399–400

    Article  CAS  PubMed  Google Scholar 

  • Hanada K, Higuchi-Takeuchi M, Okamoto M, Yoshizumi T, Shimizu M, Nakaminami K et al (2013) Small open reading frames associated with morphogenesis are hidden in plant genomes. Proc Natl Acad Sci 110(6):2395–2400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T (2007) The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21(14):1720–1725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hartford CCR, Lal A (2020) When long noncoding becomes protein coding. Mol Cell Biol 40(6)

  • Hashimoto Y, Kondo T, Kageyama Y (2008) Lilliputians get into the limelight: novel class of small peptide genes in morphogenesis. Dev Growth Differ 50:S269–S276

    Article  CAS  PubMed  Google Scholar 

  • Hazarika RR, Sostaric N, Sun Y, Van Noort V (2018) Large-scale docking predicts that sORF-encoded peptides may function through protein-peptide interactions in Arabidopsis thaliana. PLoS ONE 13(10):e0205179

    Article  PubMed  PubMed Central  Google Scholar 

  • Higuchi-Takeuchi M, Kondo T, Shimizu M, Kim YW, Shinozaki K, Hanada K (2020) Effect of small coding genes on the circadian rhythms under elevated CO 2 conditions in plants. Plant Mol Biol 104(1):55–65

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22(8):2618–2629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosseinkhan N, Zarrineh P, Masoudi-Nejad A (2014) Analysis of genome-scale expression network in four major bacterial residents of cystic fibrosis lung. Curr Genomics 15(5):408–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Housman G, Ulitsky I (2016) Methods for distinguishing between protein-coding and long noncoding RNAs and the elusive biological purpose of translation of long noncoding RNAs. Biochim Biophys Acta (1859)1:31–40

    Google Scholar 

  • Hovhannisyan H, Gabaldón T (2018) Transcriptome sequencing approaches to elucidate host–microbe interactions in opportunistic human fungal pathogens. Fungal Physiol Immunopathog 193–235

  • Hrdlickova R, Toloue M, Tian B (2017) RNA-Seq methods for transcriptome analysis. Wiley Interdiscip Rev RNA 8(1):e1364

    Article  Google Scholar 

  • Hsu PY, Benfey PN (2018) Small but mighty: functional peptides encoded by small ORFs in plants. Proteomics 18(10):1700038

    Article  Google Scholar 

  • Hsu PY, Calviello L, Wu HYL, Li FW, Rothfels CJ, Ohler U, Benfey PN (2016) Super-resolution ribosome profiling reveals unannotated translation events in Arabidopsis. Proc Natl Acad Sci 113(45):E7126–E7135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubbard T, Barker D, Birney E, Cameron G, Chen Y, Clark L et al (2002) The Ensembl genome database project. Nucleic Acids Res 30(1):38–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingolia NT (2010) Genome-wide translational profiling by ribosome footprinting. Methods in enzymology, vol 470. Elsevier, Amsterdam, pp 119–142

    Google Scholar 

  • Ingolia NT (2016) Ribosome footprint profiling of translation throughout the genome. Cell 165(1):22–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324(5924):218–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingolia NT, Brar GA, Stern-Ginossar N, Harris MS, Talhouarne GJ, Jackson SE et al (2014) Ribosome profiling reveals pervasive translation outside of annotated protein-coding genes. Cell Rep 8(5):1365–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji Z (2018) RibORF: Identifying genome-wide translated open reading frames using ribosome profiling. Curr Protoc Mol Biol 124(1):e67

    Article  PubMed  PubMed Central  Google Scholar 

  • Ji Z, Song R, Regev A, Struhl K (2015) Many lncRNAs, 5’UTRs, and pseudogenes are translated and some are likely to express functional proteins. Elife 4:e08890

    Article  PubMed  PubMed Central  Google Scholar 

  • Karupannan SK, Dowlath MJH, Arunachalam KD (2020) Phytonanotechnology: Challenges and future perspectives. Phytonanotechnol Chall Prospects 303

  • Kastenmayer JP, Ni L, Chu A, Kitchen LE, Au WC, Yang H et al (2006) Functional genomics of genes with small open reading frames (sORFs) in S. cerevisiae. Genome Res 16(3):365–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khambhati K, Bhattacharjee G, Gohil N, Braddick D, Kulkarni V, Singh V (2019) Exploring the potential of cell-free protein synthesis for extending the abilities of biological systems. Front Bioeng Biotechnol 7:248

    Article  PubMed  PubMed Central  Google Scholar 

  • Khazigaleeva R, Fesenko I (2017) Biologically active peptides encoded by small open reading frames. Russ J Bioorgan Chem 43(6):617–624

    Article  CAS  Google Scholar 

  • Khitun A, Ness TJ, Slavoff SA (2019) Small open reading frames and cellular stress responses. Mol Omics 15(2):108–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Harrison PM, Cheung KH, Lan N, Echols N, Bertone P et al (2002) An integrated approach for finding overlooked genes in yeast. Nat Biotechnol 20(1):58–63

    Article  CAS  PubMed  Google Scholar 

  • Kurihara Y, Makita Y, Shimohira H, Fujita T, Iwasaki S, Matsui M (2020) Translational landscape of protein-coding and non-protein-coding RNAs upon light exposure in Arabidopsis. Plant Cell Physiol 61(3):536–545

    Article  CAS  PubMed  Google Scholar 

  • Lauressergues D, Couzigou JM, San Clemente H, Martinez Y, Dunand C, Bécard G, Combier JP (2015) Primary transcripts of microRNAs encode regulatory peptides. Nature 520(7545):90–93

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Zhu W, Chen S, Qian J, Li L (2021) Genome-wide identification and characterization of small peptides in maize. Front Plant Sci 12:1162

    Article  Google Scholar 

  • Lin MF, Jungreis I, Kellis M (2011) PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 27(13):i275–i282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Mehdi S, Topping J, Friml J, Lindsey K (2013) Interaction of PLS and PIN and hormonal crosstalk in Arabidopsis root development. Front Plant Sci 4:75

    Article  PubMed  PubMed Central  Google Scholar 

  • Lobbestael E, Reumers V, Ibrahimi A, Paesen K, Thiry I, Gijsbers R et al (2010) Immunohistochemical detection of transgene expression in the brain using small epitope tags. BMC Biotechnol 10(1):1–10

    Article  Google Scholar 

  • Mackowiak SD, Zauber H, Bielow C, Thiel D, Kutz K, Calviello L, Obermayer B (2015) Extensive identification and analysis of conserved small ORFs in animals. Genome Biol 16(1):1–21

    Article  Google Scholar 

  • Magny EG, Pueyo JI, Pearl FM, Cespedes MA, Niven JE, Bishop SA, Couso JP (2013) Conserved regulation of cardiac calcium uptake by peptides encoded in small open reading frames. Science 341(6150):1116–1120

    Article  CAS  PubMed  Google Scholar 

  • Makarewich CA, Olson EN (2017) Mining for micropeptides. Trends Cell Biol 27(9):685–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malhi GS, Kaur M, Kaushik P, Alyemeni MN, Alsahli AA, Ahmad P (2021) Arbuscular mycorrhiza in combating abiotic stresses in vegetables: An eco-friendly approach. Saudi J Biol Sci 28(2):1465

    Article  CAS  PubMed  Google Scholar 

  • Malone B, Atanassov I, Aeschimann F, Li X, Großhans H, Dieterich C (2017) Bayesian prediction of RNA translation from ribosome profiling. Nucleic Acids Res 45(6):2960–2972

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martin SA, Dehler CE, Król E (2016) Transcriptomic responses in the fish intestine. Dev Comp Immunol 64:103–117

    Article  CAS  PubMed  Google Scholar 

  • Martinez TF, Chu Q, Donaldson C, Tan D, Shokhirev MN, Saghatelian A (2020) Accurate annotation of human protein-coding small open reading frames. Nat Chem Biol 16(4):458–468

    Article  CAS  PubMed  Google Scholar 

  • Matsubayashi Y (2011) Small post-translationally modified peptide signals in Arabidopsis. Arabidopsis Book/Am Soc Plant Biologists 9

  • Menschaert G, Van Criekinge W, Notelaers T, Koch A, Crappé J, Gevaert K, Van Damme P (2013) Deep proteome coverage based on ribosome profiling aids mass spectrometry-based protein and peptide discovery and provides evidence of alternative translation products and near-cognate translation initiation events. Mol Cell Proteom 12(7):1780–1790

    Article  CAS  Google Scholar 

  • Mewalal R, Yin H, Hu R, Jawdy S, Vion P, Tuskan GA et al (2019) Identification of Populus small RNAs responsive to mutualistic interactions with mycorrhizal fungi, Laccaria bicolor and Rhizophagus irregularis. Front Microbiol 10:515

    Article  PubMed  PubMed Central  Google Scholar 

  • Michel AM, Baranov PV (2013) Ribosome profiling: a Hi-Def monitor for protein synthesis at the genome-wide scale. Wiley Interdiscip Rev RNA 4(5):473–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michel AM, Choudhury KR, Firth AE, Ingolia NT, Atkins JF, Baranov PV (2012) Observation of dually decoded regions of the human genome using ribosome profiling data. Genome Res 22(11):2219–2229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nanjo Y, Maruyama K, Yasue H, Yamaguchi-Shinozaki K, Shinozaki K, Komatsu S (2011) Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Mol Biol 77(1–2):129–144

    Article  CAS  PubMed  Google Scholar 

  • Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, Fukuda H et al (2004) Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J 38(4):699–713

    Article  CAS  PubMed  Google Scholar 

  • Narrandes S, Xu W (2018) Gene expression detection assay for cancer clinical use. J Cancer 9(13):2249

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y (2017) Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat Plants 3(4):1–6

    Article  Google Scholar 

  • Olexiouk V, Van Criekinge W, Menschaert G (2018) An update on sORFs. org: a repository of small ORFs identified by ribosome profiling. Nucleic Acids Res 46(D1):D497–D502

    Article  CAS  PubMed  Google Scholar 

  • Orr MW, MaoY SG, Qian SB (2020) Alternative ORFs and small ORFs: shedding light on the dark proteome. Nucleic Acids Res 48(3):1029–1042

    Article  CAS  PubMed  Google Scholar 

  • Pauli A, Norris ML, Valen E, Chew GL, Gagnon JA, Zimmerman S et al. (2014) Toddler: an embryonic signal that promotes cell movement via Apelin receptors. Science 343(6172)

  • Payne SH (2015) The utility of protein and mRNA correlation. Trends Biochem Sci 40(1):1–3

    Article  CAS  PubMed  Google Scholar 

  • Pearce G (1991) A polypeptide from tomato leaves activates the expression of proteinase inhibitor genes. Science 253:895–897

    Article  CAS  PubMed  Google Scholar 

  • Peeters MK, Menschaert G (2020) The hunt for sORFs: a multidisciplinary strategy. Exp Cell Res 391(1):111923

    Article  CAS  PubMed  Google Scholar 

  • Prelich G (2012) Gene overexpression: uses, mechanisms, and interpretation. Genetics 190(3):841–854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quan M, Chen J, Zhang D (2015) Exploring the secrets of long noncoding RNAs. Int J Mol Sci 16(3):5467–5496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raj A, Wang SH, Shim H, Harpak A, Li YI, Engelmann B et al (2016) Thousands of novel translated open reading frames in humans inferred by ribosome footprint profiling. Eife 5:e13328

    Google Scholar 

  • Rasheed S, Bashir K, Nakaminami K, Hanada K, Matsui A, Seki M (2016) Drought stress differentially regulates the expression of small open reading frames (sORFs) in Arabidopsis roots and shoots. Plant Signal Behav 11(8):e1215792

    Article  PubMed  PubMed Central  Google Scholar 

  • Röhrig H, Schmidt J, Miklashevichs E, Schell J, John M (2002) Soybean ENOD40 encodes two peptides that bind to sucrose synthase. Proc Natl Acad Sci 99(4):1915–1920

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Orera J, Albà MM (2019) Translation of small open reading frames: roles in regulation and evolutionary innovation. Trends Genet 35(3):186–198

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Orera J, Messeguer X, Subirana JA, Alba MM (2014) Long non-coding RNAs as a source of new peptides. elife 3:e03523

  • Saghatelian A, Couso JP (2015) Discovery and characterization of smORF-encoded bioactive polypeptides. Nat Chem Biol 11(12):909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sallam T, Sandhu J, Tontonoz P (2018) Long noncoding RNA discovery in cardiovascular disease: decoding form to function. Circ Res 122(1):155–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheidler CM, Kick LM, Schneider S (2019) Ribosomal peptides and small proteins on the rise. ChemBioChem 20(12):1479–1486

    Article  CAS  PubMed  Google Scholar 

  • Schlesinger D, Elsässer SJ (2021) Revisiting sORFs: overcoming challenges to identify and characterize functional microproteins. FEBS J

  • Sharp PM, Li WH (1987) The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15(3):1281–1295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sipila P, Jalkanen J, Huhtaniemi IT, Poutanen M (2009) Novel epididymal proteins as targets for the development of post-testicular male contraception. Reproduction 137(3):379

    Article  CAS  PubMed  Google Scholar 

  • Skarshewski A, Stanton-Cook M, Huber T, Al Mansoori S, Smith R, Beatson SA, Rothnagel JA (2014) uPEPperoni: an online tool for upstream open reading frame location and analysis of transcript conservation. BMC Bioinform 15(1):1–6

    Article  Google Scholar 

  • Slavoff SA, Mitchell AJ, Schwaid AG, Cabili MN, Ma J, Levin JZ et al (2013) Peptidomic discovery of short open reading frame–encoded peptides in human cells. Nat Chem Biol 9(1):59–64

    Article  CAS  PubMed  Google Scholar 

  • Smith JE, Alvarez-Dominguez JR, Kline N, Huynh NJ, Geisler S, Hu W et al (2014) Translation of small open reading frames within unannotated RNA transcripts in Saccharomyces cerevisiae. Cell Rep 7(6):1858–1866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song B, Jiang M, Gao L (2021) RiboNT: a noise-tolerant predictor of open reading frames from ribosome-protected footprints. Life 11(7):701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sousa ME, Farkas MH (2018) Micropeptide. PLoS Genet 14(12):e1007764

    Article  PubMed  PubMed Central  Google Scholar 

  • Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y (2014) Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346(6207):343–346

    Article  CAS  PubMed  Google Scholar 

  • Takahashi F, Hanada K, Kondo T, Shinozaki K (2019) Hormone-like peptides and small coding genes in plant stress signaling and development. Curr Opin Plant Biol 51:88–95

    Article  CAS  PubMed  Google Scholar 

  • Tinafar A, Jaenes K, Pardee K (2019) Synthetic biology goes cell-free. BMC Biol 17(1):1–14

    Article  CAS  Google Scholar 

  • Vanderperre B, Lucier JF, Bissonnette C, Motard J, Tremblay G, Vanderperre S et al. (2013) Direct detection of alternative open reading frames translation products in human significantly expands the proteome. PloS one 8(8):e70698

  • Wang D, Li C, Zhao Q, Zhao L, Wang M, Zhu D et al (2009) Zm401p10, encoded by an anther-specific gene with short open reading frames, is essential for tapetum degeneration and anther development in maize. Funct Plant Biol 36(1):73–85

    Article  PubMed  Google Scholar 

  • Wang P, Lombi E, Zhao FJ, Kopittke PM (2016) Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci 21(8):699–712

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Wang Y, Xie Z (2019) Computational resources for ribosome profiling: from database to Web server and software. Brief Bioinform

  • Wheeler DL, Church DM, Lash AE, Leipe DD, Madden TL, Pontius JU et al (2001) Database resources of the national center for biotechnology information. Nucleic Acids Res 29(1):11–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao Z, Huang R, Xing X, Chen Y, Deng H, Yang X (2018) De novo annotation and characterization of the translatome with ribosome profiling data. Nucleic Acids Res 46(10):e61–e61

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu S (2017) Transcriptome profiling in systems vascular medicine. Front Pharmacol 8:563

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Z, Hu L, Shi B, Geng S, Xu L, Wang D, Lu ZJ (2018) Ribosome elongating footprints denoised by wavelet transform comprehensively characterize dynamic cellular translation events. Nucleic Acids Res 46(18):e109–e109

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamashita Y, Takamatsu S, Glasbrenner M, Becker T, Naito S, Beckmann R (2017) Sucrose sensing through nascent peptide-meditated ribosome stalling at the stop codon of Arabidopsis bZIP 11 uORF 2. FEBS Lett 591(9):1266–1277

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Tschaplinski TJ, Hurst GB, Jawdy S, Abraham PE, Lankford PK et al (2011) Discovery and annotation of small proteins using genomics, proteomics, and computational approaches. Genome Res 21(4):634–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang X, Jensen SI, Wulff T, Harrison SJ, Long KS (2016) Identification and validation of novel small proteins in Pseudomonas putida. Environ Microbiol Rep 8(6):966–974

    Article  CAS  PubMed  Google Scholar 

  • Ye M, Zhang J, Wei M, Liu B, Dong K (2020) Emerging role of long noncoding RNA-encoded micropeptides in cancer. Cancer Cell Int 20(1):1–9

    Article  CAS  Google Scholar 

  • Yeasmin F, Yada T, Akimitsu N (2018) Micropeptides encoded in transcripts previously identified as long noncoding RNAs: a new chapter in transcriptomics and proteomics. Front Genet 9:144

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin X, Jing Y, Xu H (2019) Mining for missed sORF-encoded peptides. Expert Rev Proteomic 16(3):257–266

    Article  CAS  Google Scholar 

  • Yu SH, Vogel J, Förstner KU (2018) ANNOgesic: a Swiss army knife for the RNA-seq based annotation of bacterial/archaeal genomes. GigaScience 7(9):giy096

    Article  PubMed Central  Google Scholar 

  • Yu SH (2019) Development and application of computational tools for RNA-Seq based transcriptome annotations. Bayerische Julius-Maximilians-Universitaet Wuerzburg (Germany).

  • Zemella A, Thoring L, Hoffmeister C, Kubick S (2015) Cell-free protein synthesis: pros and cons of prokaryotic and eukaryotic systems. ChemBioChem 16(17):2420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang JZ (2003) Overexpression analysis of plant transcription factors. Curr Opin Plant Biol 6(5):430–440

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, He D, Xu Y, Hou J, Pan BF, Wang Y et al (2017) Genome-wide identification and differential analysis of translational initiation. Nat Commum 8(1):1–14

    Google Scholar 

  • Zhu M, Gribskov M (2019) MiPepid: MicroPeptide identification tool using machine learning. BMC Bioinformatics 20(1):1–11

    Article  Google Scholar 

  • Zhu Y, Orre LM, Johansson HJ, Huss M, Boekel J, Vesterlund M et al (2018) Discovery of coding regions in the human genome by integrated proteogenomics analysis workflow. Nat Commun 9(1):1–14

    Google Scholar 

  • Zordan RE, Beliveau BJ, Trow JA, Craig NL, Cormack BP (2015) Avoiding the ends: internal epitope tagging of proteins using transposon Tn7. Genetics 200(1):47–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was funded by the Ministry of Higher Education, Malaysia, under the Fundamental Research Grant Scheme (FRGS), Grant No: FRGS/1/2019/STG05/UM/02/3.

Author information

Authors and Affiliations

  1. Centre for Research in Biotechnology for Agriculture (CEBAR), Universiti Malaya, 50603, Kuala Lumpur, Malaysia

    Sheue Ni Ong, Boon Chin Tan & Chee How Teo

  2. Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603, Kuala Lumpur, Malaysia

    Aisyafaznim Al-Idrus

Authors
  1. Sheue Ni Ong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Boon Chin Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aisyafaznim Al-Idrus
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chee How Teo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CHT conceived the idea. SNO wrote the manuscript. CHT, BCT, and AAI reviewed and gave suggestions to improve the manuscript.

Corresponding author

Correspondence to Chee How Teo.

Ethics declarations

Conflict of interest

No potential conflict of interest was reported by the authors.

Ethics approval

Not applicable.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ong, S.N., Tan, B.C., Al-Idrus, A. et al. Small open reading frames in plant research: from prediction to functional characterization. 3 Biotech 12, 76 (2022). https://doi.org/10.1007/s13205-022-03147-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-022-03147-w

Keywords

Search

Navigation