Large-scale discovery of non-conventional peptides in grape (Vitis vinifera L.) through peptidogenomics

Mao-Song Pei , Hai-Nan Liu , Tong-Lu Wei , Yi-He Yu , Da-Long Guo

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac023

PDF (745KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac023 DOI: 10.1093/hr/uhac023
Article
research-article
Large-scale discovery of non-conventional peptides in grape (Vitis vinifera L.) through peptidogenomics
Author information +
History +
PDF (745KB)

Abstract

Non-conventional peptides (NCPs), which are peptides derived from previously unannotated coding sequences, play important biological roles in plants. In this study, we used peptidogenomic methods that integrated mass spectrometry (MS) peptidomics and a six-frame translation database to extensively identify NCPs in grape. In total, 188 and 2021 non-redundant peptides from the Arabidopsis thaliana and Vitis vinifera L. protein database at Ensembl/URGI and an individualized peptidogenomic database were identified. Unlike conventional peptides, these NCPs derived mainly from intergenic, intronic, upstream ORF, 5UTR, 3UTR, and downstream ORF regions. These results show that unannotated regions are translated more broadly than we thought. We also found that most NCPs were derived from regions related to phenotypic variations, LTR retrotransposons, and domestication selection, indicating that the NCPs have an important function in complex biological processes. We also found that the NCPs were developmentally specific and had transient and specific functions in grape berry development. In summary, our study is the first to extensively identify NCPs in grape. It demonstrated that there was a large amount of translation in the genome. These results lay a foundation for studying the functions of NCPs and also provide a reference for the discovery of new functional genes in grape.

Cite this article

Download citation ▾
Mao-Song Pei, Hai-Nan Liu, Tong-Lu Wei, Yi-He Yu, Da-Long Guo. Large-scale discovery of non-conventional peptides in grape (Vitis vinifera L.) through peptidogenomics. Horticulture Research, 2022, 9 (1) : uhac023 DOI:10.1093/hr/uhac023

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Wang S, Tian L, Liu H et al. Large-scale discovery of non-conventional peptides in maize and Arabidopsis through an integrated peptidogenomic pipeline. Mol Plant. 2020; 13: 1078-93.

[2]

Qu LJ, Li L, Lan Z et al. Peptide signaling during the pollen tube journey and double fertilization. J Exp Bot. 2015; 66: 5139-50.

[3]

Casson SA, Chilley PM, Topping JF et al. The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell. 2002; 14: 1705-21.

[4]

Narita NN, Moore S, Horiguchi G et al. Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana . Plant J. 2004; 38: 699-713.

[5]

De Coninck B, Carron D, Tavormina P et al. Mining the genome of Arabidopsis thaliana as a basis for the identification of novel bioactive peptides involved in oxidative stress tolerance. J Exp Bot. 2013; 64: 5297-307.

[6]

Chen QJ, Deng BH, Gao J et al. A miRNA-encoded small peptide, vvi-miPEP171d1, regulates adventitious root formation. Plant Physiol. 2020; 183: 656-70.

[7]

Lauressergues D, Couzigou JM, Clemente HS et al. Primary transcripts of microRNAs encode regulatory peptides. Nature. 2015; 520: 90-3.

[8]

Vale M, Rodrigues J, Badim H et al. Exogenous application of non-mature miRNA-encoded miPEP164c inhibits proanthocyanidin synthesis and stimulates anthocyanin accumulation in grape berry cells. Front Plant Sci. 2021; 12: 706679.

[9]

Mackowiak SD, Zauber H, Bielow C et al. Extensive identification and analysis of conserved small ORFs in animals. Genome Biol. 2015; 16: 179.

[10]

Aspden JL, Eyre-Walker YC, Phillips RJ et al. Extensive translation of small open Reading frames revealed by poly-Ribo-Seq. elife. 2014; 3: e03528.

[11]

Galindo MI, Pueyo JI, Fouix S et al. Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol. 2007; 5: e106.

[12]

Liang Y, Zhu W, Chen S et al. Genome-wide identification and characterization of small peptides in maize. Front Plant Sci. 2021; 12: 695439.

[13]

Lease KA, Walker JC . The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics . Plant Physiol. 2006; 142: 831-8.

[14]

Makarewich CA, Olson EN . Mining for Micropeptides. Trends Cell Biol. 2017; 27: 685-96.

[15]

Coombe BG . Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res. 1995; 1: 104-10.

[16]

Rice P, Longden I, Bleasby A . EMBOSS: the European molecular biology open software suite. Trends Genet. 2000; 16: 276-7.

[17]

Starck SR, Tsai JC, Chen K et al. Translation from the 5 untranslated region shapes the integrated stress response . Science. 2016; 351: aad3867.

[18]

Na CH, Barbhuiya MA, Kim MS et al. Discovery of noncanonical translation initiation sites through mass spectrometric analysis of protein N termini. Genome Res. 2018; 28: 25-36.

[19]

Zhang HL, Wang ZG, Yu YH et al. Genome-wide identification and characterization of long non-coding RNAs involved in grape berry ripening. J Berry Res. 2020; 10: 475-96.

[20]

Thorvaldsdóttir H, Robinson JT, Mesirov JP . Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 2013; 14: 178-92.

[21]

Delfino P, Zenoni S, Imanifard Z et al. Selection of candidate genes controlling veraison time in grapevine through integration of meta-QTL and transcriptomic data. BMC Genomics. 2020; 20: 739.

[22]

Ma T, Wei X, Zhang Y et al. Development of molecular markers based on LTR retrotransposon in the Cleistogenes songorica genome. J Appl Genet. 2021.

[23]

Liang Z, Duan S, Sheng J et al. Author correction: whole-genome resequencing of 472 Vitis accessions for grapevine diversity and demographic history analyses. Nat Commun. 2020; 11: 2341.

[24]

Kui L, Tang M, Duan S et al. Identification of selective sweeps in the domesticated table and wine grape (Vitis vinifera L.) . Front Plant Sci. 2020; 11: 572.

[25]

Zou C, Massonnet M, Minio A et al. Multiple independent recombinations led to hermaphroditism in grapevine. Proc Natl Acad Sci U S A. 2021; 118: e2023548118.

[26]

Guo DL, Zhao HL, Li Q et al. Genome-wide association study of berry-related traits in grape (Vitis vinifera L.) based on genotyping-by-sequencing markers . Hortic Res. 2019; 6: 11.

[27]

Castellana N, Bafna V . Proteogenomics to discover the full coding content of genomes: a computational perspective. J Proteome. 2010; 73: 2124-35.

[28]

Woo S, Cha SW, Merrihew G et al. Proteogenomic database construction driven from large scale RNA-seq data. J Proteome Res. 2014; 13: 21-8.

[29]

Yang MK, Lin X, Liu X et al. Genome annotation of a model diatom Phaeodactylum tricornutum using an integrated proteogenomic pipeline . Mol Plant. 2018; 11: 1292-307.

[30]

Nesvizhskii AI . Proteogenomics: concepts, applications and computational strategies. Nat Methods. 2014; 11: 1114-25.

[31]

Kersten RD, Yang YL, Xu Y et al. A mass spectrometry-guided genome mining approach for natural product peptidogenomics. Nat Chem Biol. 2011; 7: 794-802.

[32]

Mohimani H, Pevzner PA . Dereplication, sequencing and identification of peptidic natural products: from genome mining to peptidogenomics to spectral networks. Nat Prod Rep. 2016; 33: 73-86.

[33]

Slavoff SA, Mitchell AJ, Schwaid AG et al. Peptidomic discovery of short open reading frame-encoded peptides in human cells. Nat Chem Biol. 2013; 9: 59-64.

[34]

Huang JZ, Chen M, Chen D et al. A peptide encoded by a putative lncRNA HOXB-AS3 suppresses colon cancer growth. Mol Cell. 2017; 68: 171-84.

[35]

Nelson BR, Makarewich CA, Anderson DM et al. A peptide encoded by a transcript annotated as long noncoding RNA enhances SERCA activity in muscle. Science. 2016; 351: 271-5.

[36]

Lun YZ, Pan ZP, Liu SA et al. The peptide encoded by a novel putative lncRNA HBVPTPAP inducing the apoptosis of hepatocellular carcinoma cells by modulating JAK/STAT signaling pathways. Virus Res. 2020; 287: 198104.

[37]

Fesenko I, Kirov I, Kniazev A et al. Distinct types of short open reading frames are translated in plant cells. Genome Res. 2019; 29: 1464-77.

[38]

Jorgensen RA, Dorantes-Acosta AE . Conserved peptide upstream open Reading frames are associated with regulatory genes in angiosperms. Front Plant Sci. 2012; 3: 191.

[39]

von Arnim AG, Jia Q, Vaughn JN . Regulation of plant translation by upstream open reading frames. Plant Sci. 2014; 214: 1-12.

[40]

Hsu PY, Benfey PN . Small but mighty: functional peptides encoded by small ORFs in plants. Proteomics. 2018; 18: e1700038.

[41]

Noh AL, Watanabe S, Takahashi H et al. An upstream open reading frame represses expression of a tomato homologue of Arabidopsis ANAC096, a NAC domain transcription factor gene, in a peptide sequence dependent manner. Plant Biotechnol. 2015; 32: 157-63.

[42]

Li Z, Fu Y, Shen J et al. Upstream open Reading frame mediated translation of WNK8 is required for ABA response in Arabidopsis . Int J Mol Sci. 2021; 22: 10683.

[43]

Clark RM, Wagler TN, Quijada P et al. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet. 2006; 38: 594-7.

[44]

Castelletti S, Tuberosa R, Pindo M et al. A MITE transposon insertion is associated with differential methylation at the maize flowering time QTL Vgt1. G3 (Bethesda). 2014; 4: 805-12.

[45]

Zhao M, Ma J . Co-evolution of plant LTR-retrotransposons and their host genomes. Protein Cell. 2013; 4: 493-501.

[46]

Canaguier A, Grimplet J, Di Gaspero et al . A new version of the grapevine reference genome assembly (12X.v2) and of its annotation (VCost.v3). Genom Data. 2017; 14: 56-62.

[47]

Cheng CY, Krishnakumar V, Chan AP et al. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 2017; 89: 789-804.

[48]

Quinlan AR, Hall IM . BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010; 26: 841-2.

[49]

Hao Z, Lv D, Ge Y et al. RIdeogram: drawing SVG graphics to visualize and map genome-wide data on the idiograms. PeerJ Comput Sci. 2020; 6: e251.

[50]

Ellinghaus D, Kurtz S, Willhoeft U . LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC bioinform. 2008; 9: 18.

[51]

Xu Z, Wang H . LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007; 35: W265-8.

PDF (745KB)

56

Accesses

0

Citation

Detail

Sections
Recommended

/