植物小开放阅读框编码肽的研究进展

陈燕君; 王坤

doi:10.11913/PSJ.2095-0837.2020.50707

植物小开放阅读框编码肽的研究进展

陈燕君,
王坤^,

武汉大学生命科学学院, 武汉 430072

基金项目:

中央高校基本科研业务费专项（2042018kf0225）。

详细信息

作者简介:
陈燕君(1995-),女,硕士研究生,研究方向为植物发育生物学(E-mail:chenyj@whu.edu.cn)。

通讯作者:
王坤,E-mail:wangk05@whu.edu.cn

中图分类号: Q943.2
计量
- 文章访问数: 696
- HTML全文浏览量: 17
- PDF下载量: 1030
出版历程
- 收稿日期: 2020-03-29
- 修回日期: 2020-04-23
- 网络出版日期: 2022-10-31
- 发布日期: 2020-10-27

Advances in studies on small open reading frames in plants

Chen Yan-Jun,
Wang Kun^,

College of Life Sciences, Wuhan University, Wuhan 430072, China

Funds:

This work was supported by a grant from the Fundamental Research Funds for the Central Universities (2042018kf0225).

摘要

摘要: 小开放阅读框（small open reading frame，sORF）一般指基因组中能够编码长度在100个氨基酸左右或以内短肽的开放阅读框。它们广泛存在于植物基因组，却因编码短肽而常被基因组注释忽视。随着翻译组学和蛋白质组学测序技术的发展，具有翻译活性的sORF被证实广泛存在于植物基因组，且参与植物生长发育等重要过程的调控。该文归纳了近些年来植物领域sORF的一些研究进展，主要包括sORF的来源与分类、信息学预测方法和生物学功能等，并基于此对植物sORF未来的研究方向进行了展望。
- 小开放阅读框 /
- 植物 /
- 注释 /
- 调控
Abstract: Small open reading frames (sORFs) can encode small peptides with lengths of about 100 amino acids or less. They exist in plant genomes but are often excluded from genome annotations. With the development of translatomics and proteomics, accumulating evidence suggests that sORFs are widely present in plant genomes and are involved in the regulation of plant growth and development. This review summarizes recent progress in sORF studies in plants, including biogenesis and classification, bioinformatic prediction methods, and biological functions, and provides a prospective outlook for future research directions.
- Small open reading frames /
- Plants /
- Annotation /
- Regulation

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参考文献(71)

[1]	Ji Z, Song R, Regev A, Struhl K. Many lncRNAs, 5'UTRs, and pseudogenes are translated and some are likely to express functional proteins[J]. eLife, 2015, 4:e08890.
[2]	Raney A, Baron AC, Mize GJ, Law GL, Morris DR. In vitro translation of the upstream open reading frame in the mammalian mRNA encoding S-adenosylmethionine decarboxylase[J]. J Biol Chem, 2000, 275(32):24444-24450.
[3]	Couso JP, Patraquim P. Classification and function of small open reading frames[J]. Nat Rev Mol Cell Biol, 2017, 18(9):575-589.
[4]	Hsu PY, Benfey PN. Small but mighty:functional peptides encoded by small ORFs in plants[J]. Proteomics, 2018, 18(10):1700038.
[5]	Ge Z, Bergonci T, Zhao Y, Zou Y, Du S, et al. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling[J]. Science, 2017, 358(6370):1596-1600.
[6]	Zhong S, Liu M, Wang Z, Huang Q, Hou S, et al. Cys-teine-rich peptides promote interspecific genetic isolation in Arabidopsis[J]. Science, 2019, 364(6443):1-8.
[7]	Lei L, Shi J, Chen J, Zhang M, Sun S, et al. Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress[J]. Plant J, 2015, 84(6):1206-1218.
[8]	Xu G, Yuan M, Ai C, Liu L, Zhuang E, et al. uORF-mediated translation allows engineered plant disease resistance without fitness costs[J]. Nature, 2017, 545(7655):491-494.
[9]	Delay C, Imin N, Djordjevic MA. Regulation of Arabidopsis root development by small signaling peptides[J]. Front Plant Sci, 2013, 4(4):352-357.
[10]	Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, et al. A small peptide modulates stomatal control via abscisic acid in long-distance signalling[J]. Nature, 2018, 556(7700):235-241.
[11]	Chugunova A, Navalayeu T, Dontsova O, Sergiev P. Mining for Small Translated ORFs[J]. J Proteome Res, 2018, 17(1):1-11.
[12]	Zhang S, Gao J, Liu C. The role of non-coding RNAs in neurodevelopmental disorders[J]. Front Genet, 2019, 10(10):1033-1042.
[13]	Marquardt S, Raitskin O, Wu Z, Liu F, Sun Q, Dean C. Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription[J]. Mol Cell, 2014, 54(1):156-165.
[14]	Wang Y, Luo X, Sun F, Hu J, Zha X, et al. Overexpres-sing lncRNA LAIR increases grain yield and regulates neighbouring gene cluster expression in rice[J]. Nat Commun, 2018, 9(1):3516-3524.
[15]	Cui J, Luan Y, Jiang N, Bao H, Meng J. Comparative transcriptome analysis between resistant and susceptible tomato allows the identification of lncRNA16397 conferring resistance to Phytophthora infestans by co-expressing glutaredoxin[J]. Plant J, 2017, 89(3):577-589.
[16]	Ruiz-Orera J, Messeguer X, Subirana JA, Alba MM. Long non-coding RNAs as a source of new peptides[J]. eLife, 2014, 3:e03523.
[17]	Lin X, Lin W, Ku YS, Wong FL, Li MW, et al. Analysis of soybean long non-coding RNAs reveals a subset of small peptide-coding transcripts[J]. Plant Physiol, 2020, 182(3):1359-1374.
[18]	Levine MT, Jones CD, Kern AD, Lindfors HA, Begun DJ. Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression[J]. Proc Natl Acad Sci, 2006, 103(26):9935-9939.
[19]	Juntawong P, Girke T, Bazin J, Bailey-Serres J. Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis[J]. Proc Natl Acad Sci, 2014, 111(1):203-212.
[20]	Fesenko I, Kirov I, Kniazev A, Khazigaleeva R, Lazarev V, et al. Distinct types of short open reading frames are translated in plant cells[J]. Genome Res, 2019, 29(9):1464-1477.
[21]	Zhang YC, Liao JY, Li ZY, Yu Y, Zhang JP, et al. Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice[J]. Genome Biol, 2014, 15(12):512-528.
[22]	Conn VM, Hugouvieux V, Nayak A, Conos SA, Capovilla G, et al. A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation[J]. Nature Plants, 2017, 3(5):1-5.
[23]	Zhang M, Huang N, Yang X, Luo J, Yan S, et al. A novel protein encoded by the circular form of the SHPRH gene suppresses glioma tumorigenesis[J]. Oncogene, 2018, 37(13):1805-1814.
[24]	Zhang M, Zhao K, Xu X, Yang Y, Yan S, et al. A peptide encoded by circular form of LINC-PINT suppresses oncogenic transcriptional elongation in glioblastoma[J]. Nat Commun, 2018, 9(1):1-17.
[25]	Lee Y, Kim M, Han J, Yeom KH, Lee S, et al. MicroRNA genes are transcribed by RNA polymeraseⅡ[J]. EMBO J, 2004, 23(20):4051-4060.
[26]	Cui C, Wang JJ, Zhao JH, Fang YY, He XF, et al. A Brassica miRNA regulates plant growth and immunity through distinct modes of action[J]. Mol Plant, 2020, 13(2):231-245.
[27]	Yu Y, Jia T, Chen X. The ‘how’ and ‘where’ of plant microRNAs[J]. New Phytol, 2017, 216(4):1002-1017.
[28]	Tang J, Chu C. MicroRNAs in crop improvement:Fine-tuners for complex traits[J]. Nature Plants, 2017, 3(7):1-11.
[29]	Lauressergues D, Couzigou JM, San Clemente H, Marti-nez Y, Dunand C, et al. Primary transcripts of microRNAs encode regulatory peptides[J]. Nature, 2015, 520(7545):90-93.
[30]	Iacono M, Mignone F, Pesole G. uAUG and uORFs in human and rodent 5'untranslated mRNAs[J]. Gene, 2005, 349(11):97-105.
[31]	Calvo SE, Pagliarini DJ, Mootha VK. Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans[J]. Proc Natl Acad Sci, 2009, 106(18):7507-7512.
[32]	Bazzini AA, Johnstone TG, Christiano R, Mackowiak SD, Obermayer B, et al. Identification of small ORFs in vertebrates using ribosome footprinting and evolutionary conservation[J]. EMBO J, 2014, 33(9):981-993.
[33]	Weaver J, Mohammad F, Buskirk AR, Storz G. Identifying small proteins by ribosome profiling with stalled initiation complexes[J]. MBio, 2019, 10(2):e02819-18.
[34]	Wu HYL, Song GY, Walley JW, Hsu PYS. The tomato translational landscape revealed by transcriptome assembly and ribosome profiling[J]. Plant Physiol, 2019, 181(1):367-380.
[35]	Hazarika RR, De Coninck B, Yamamoto LR, Martin LR, Cammue BPA, van Noort V. ARA-PEPs:A repository of putative SORF-encoded peptides in Arabidopsis thaliana[J]. BMC Bioinformatics, 2017, 18(1):37.
[36]	Kurihara Y, Makita Y, Kawashima M, Fujita T, Iwasaki S, Matsui M. Transcripts from downstream alternative transcription start sites evade uORF-mediated inhibition of gene expression in Arabidopsis[J]. Proc Natl Acad Sci, 2018, 115(30):7831-7836.
[37]	Xu G, Greene GH, Yoo H, Liu L, Marqués J, et al. Global translational reprogramming is a fundamental layer of immune regulation in plants[J]. Nature, 2017, 545(7655):487-490.
[38]	Hanada K, Zhang X, Borevitz JO, Li WH, Shiu SH. 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[J]. Genome Res, 2007, 17(5):632-640.
[39]	Rice P, Longden I, Bleasby A. EMBOSS:the european molecular biology open software suite[J]. Trends Genet, 2000, 16(6):276-277.
[40]	Skarshewski A, Stanton-Cook M, Huber T, Al Mansoori S, Smith R, et al. UPEPperoni:An online tool for upstream open reading frame location and analysis of transcript conservation[J]. BMC Bioinformatics, 2014, 15(1):36-42.
[41]	Wang J, Gribskov M. IRESpy:An XGBoost model for prediction of internal ribosome entry sites[J]. BMC Bioinformatics, 2019, 20(1):409-422.
[42]	Zhao J, Wu J, Xu T, Yang Q, He J, Song X. IRESfinder:identifying RNA internal ribosome entry site in eukaryotic cell using framed k-mer features[J]. Journal of Genetics and Genomics, 2018, 45(7):403-406.
[43]	Wu TY, Hsieh CC, Hong JJ, Chen CY, Tsai YS. IRSS:A web-based tool for automatic layout and analysis of IRES secondary structure prediction and searching system in silico[J]. BMC Bioinformatics, 2009, 10(1):160-173.
[44]	Hong JJ, Wu TY, Chang TY, Chen CY. Viral IRES prediction system-a web server for prediction of the IRES secondary structure in silico[J]. PLoS One, 2013, 8(11):e79288.
[45]	Kolekar P, Pataskar A, Kulkarni-Kale U, Pal J, Kulkarni A. IRESPred:web server for prediction of cellular and viral internal ribosome entry site (IRES)[J]. Sci Rep, 2016, 6(1):1-7.
[46]	Zhu MM, Gribskov M. MiPepid:MicroPeptide identification tool using machine learning[J]. BMC Bioinformatics, 2019, 20:559.
[47]	Malone B, Atanassov I, Aeschimann F, Li X, Großhans H, Dieterich C. Bayesian prediction of RNA translation from ribosome profiling[J]. Nucleic Acids Res, 2017, 45(6):2960-2972.
[48]	Xiao Z, Huang R, Xing X, Chen Y, Deng H, Yang X. De novo annotation and characterization of the translatome with ribosome profiling data[J]. Nucleic Acids Res, 2018, 46(10):e61.
[49]	Erhard F, Halenius A, Zimmermann C, L'Hernault A, Kowalewski DJ, et al. Improved Ribo-seq enables identification of cryptic translation events[J]. Nat Methods, 2018, 15(5):363-366.
[50]	Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification[J]. Nat Biotechnol, 2008, 26(12):1367-1372.
[51]	Vaudel M, Barsnes H, Berven FS, Sickmann A, Martens L. SearchGUI:An open-source graphical user interface for simultaneous OMSSA andX!Tandem searches[J]. Proteomics, 2011, 11(5):996-999.
[52]	Spealman P, Naik AW, May GE, Kuersten S, Freeberg L, et al. Conserved non-AUG uORFs revealed by a novel regression analysis of ribosome profiling data[J]. Genome Res, 2018, 28(2):214-222.
[53]	Jorgensen RA, Dorantes-Acosta AE. Conserved peptide upstream open reading frames are associated with regulatory genes in angiosperms[J]. Front Plant Sci, 2012, 3(191):191-202.
[54]	Hsu PY, Calviello L, Wu HYL, Li FW, Rothfels CJ, et al. Super-resolution ribosome profiling reveals unannotated translation events in Arabidopsis[J]. Proc Natl Acad Sci, 2016, 113(45):7126-7135.
[55]	Tran MK, Schultz CJ, Baumann U. Conserved upstream open reading frames in higher plants[J]. BMC Genomics, 2008, 9(9):361-378.
[56]	Hao Y, Zhang L, Niu Y, Cai T, Luo J, et al. SmProt:a database of small proteins encoded by annotated coding and non-coding RNA loci[J]. Brief Bioinform, 2018, 19(4):636-643.
[57]	Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS. Genome-wide analysis in vivo of translation with nuc-leotide resolution using ribosome profiling[J]. Science, 2009, 324(5924):218-223.
[58]	Guttman M, Russell P, Ingolia NT, Weissman JS, Lander ES. Ribosome profiling provides evidence that large non-coding RNAs do not encode proteins[J]. Cell, 2014, 154(1):240-251.
[59]	Zhang B, Wang J, Wang X, Zhu J, Liu Q, et al. Proteo-genomic characterization of human colon and rectal cancer[J]. Nature, 2014, 513(7518):382-387.
[60]	Kim MS, Pinto SM, Getnet D, Nirujogi RS, Manda SS, et al. A draft map of the human proteome[J]. Nature, 2014, 509(7502):575-581.
[61]	Baerenfaller K, Grossmann J, Grobei MA, Hull R, Hirsch-hoffmann M, et al. Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics[J]. Science, 2008, 320(5878):938-941.
[62]	Budamgunta H, Olexiouk V, Luyten W, Schildermans K, Maes E, et al. Comprehensive peptide analysis of mouse brain striatum identifies novel sORF-encoded polypeptides[J]. Proteomics, 2018, 18(10):1700218-1700234.
[63]	Khitun A, Slavoff SA. Proteomic detection and validation of translated small open reading frames[J]. Curr Protoc Chem Biol, 2019, 11(4):77-104.
[64]	Röhrig H, Schmidt J, Miklashevichs E, Schell J, John M. Soybean ENOD40 encodes two peptides that bind to sucrose synthase[J]. Proc Natl Acad Sci, 2002, 99(4):1915-1920.
[65]	Dong X, Wang D, Liu P, Li C, Zhao Q, et al. Zm908p11, encoded by a short open reading frame (sORF) gene, functions in pollen tube growth as a profilin ligand in maize[J]. J Exp Bot, 2013, 64(8):2359-2372.
[66]	Wang D, Li C, Zhao Q, Zhao L, Wang M, et al. Zm401p10, encoded by an anther-specific gene with short open reading frames, is essential for tapetum degeneration and anther development in maize[J]. Funct Plant Biol, 2009, 36(1):73-85.
[67]	Saul H, Elharrar E, Gaash R, Eliaz D, Valenci M, et al. The upstream open reading frame of the Arabidopsis AtMHX gene has a strong impact on transcript accumulation through the nonsense-mediated mRNA decay pathway[J]. Plant J, 2009, 60(6):1031-1042.
[68]	Alatorre-Cobos F, Cruz-Ramírez A, Hayden CA, Pérez-Torres CA, Chauvin AL, et al. Translational regulation of Arabidopsis XIPOTL1 is modulated by phosphocholine levels via the phylogenetically conserved upstream open reading frame 30[J]. J Exp Bot, 2012, 63(14):5203-5221.
[69]	Rahmani F, Hummel M, Schuurmans J, Wiese-Klinkenberg A, Smeekens S, Hanson J. Sucrose control of translation mediated by an upstream open reading frame-encoded peptide[J]. Plant Physiol, 2009, 150(3):1356-1367.
[70]	Si X, Zhang H, Wang Y, Chen K, Gao C. Manipulating gene translation in plants by CRISPR-Cas9-mediated genome editing of upstream open reading frames[J]. Nat Protoc, 2020, 15(2):338-363.
[71]	Zhong S, Liu M, Wang Z, Huang Q, Hou S, X et al. Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis[J]. Science, 2019, 364(6443):9564-9571.

施引文献(5)

期刊类型引用(2)

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