Transfer RNA and ribosomal RNA fragments - emerging players in plant-microbe interactions.
cross-kingdom transfer
extracellular vesicle
gene silencing
plant-microbe interaction
rRNA fragment
tRNA fragment
translation inhibition
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
20 Nov 2023
20 Nov 2023
Historique:
received:
20
09
2023
accepted:
03
11
2023
medline:
21
11
2023
pubmed:
21
11
2023
entrez:
20
11
2023
Statut:
aheadofprint
Résumé
According to current textbooks, the principal task of transfer and ribosomal RNAs (tRNAs and rRNAs, respectively) is synthesizing proteins. During the last decade, additional cellular roles for precisely processed tRNA and rRNAs fragments have become evident in all kingdoms of life. These RNA fragments were originally overlooked in transcriptome datasets or regarded as unspecific degradation products. Upon closer inspection, they were found to engage in a variety of cellular processes, in particular the modulation of translation and the regulation of gene expression by sequence complementarity- and Argonaute protein-dependent gene silencing. More recently, the presence of tRNA and rRNA fragments has also been recognized in the context of plant-microbe interactions, both on the plant and the microbial side. While most of these fragments are likely to affect endogenous processes, there is increasing evidence for their transfer across kingdoms in the course of such interactions; these processes may involve mutual exchange in association with extracellular vesicles. Here, we summarize the state-of-the-art understanding of tRNA and rRNA fragment's roles in the context of plant-microbe interactions, their potential biogenesis, presumed delivery routes, and presumptive modes of action.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Alexander von Humboldt-Stiftung
ID : GBR 1204122 GSA
Organisme : Deutsche Forschungsgemeinschaft
ID : 433194101
Organisme : Leverhulme Trust
ID : RF-2019-053
Organisme : RWTH Aachen University
Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
Alves CS, Nogueira FTS. 2021. Plant small RNA world growing bigger: tRNA-derived fragments, longstanding players in regulatory processes. Frontiers in Molecular Biosciences 8: 638911.
Alves CS, Vicentini R, Duarte GT, Pinoti VF, Vincentz M, Nogueira FTS. 2017. Genome-wide identification and characterization of tRNA-derived RNA fragments in land plants. Plant Molecular Biology 93: 35-48.
Asha S, Soniya EV. 2016. Transfer RNA derived small RNAs targeting defense responsive genes are induced during Phytophthora capsici infection in black pepper (Piper nigrum L.). Frontiers in Plant Science 7: 767.
Asha S, Soniya EV. 2017. The sRNAome mining revealed existence of unique signature small RNAs derived from 5.8SrRNA from Piper nigrum and other plant lineages. Scientific Reports 7: 41052.
Åsman AKM, Vetukuri RR, Jahan SN, Fogelqvist J, Corcoran P, Avrova AO, Whisson SC, Dixelius C. 2014. Fragmentation of tRNA in Phytophthora infestans asexual life cycle stages and during host plant infection. BMC Microbiology 14: 308.
Avcilar-Kucukgoze I, Kashina A. 2020. Hijacking tRNAs from translation: regulatory functions of tRNAs in mammalian cell physiology. Frontiers in Molecular Biosciences 7: 610617.
Baldrich P, Meyers BC. 2019. Bacteria send messages to colonize plant roots. Science 365: 868-869.
Cai Q, Qiao L, Wang M, He B, Lin F-M, Palmquist J, Huang H-D, Jin H. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360: 1126-1129.
Chen C-J, Liu Q, Zhang Y-C, Qu L-H, Chen Y-Q, Gautheret D. 2011. Genome-wide discovery and analysis of microRNAs and other small RNAs from rice embryogenic callus. RNA Biology 8: 538-547.
Chen Z, Sun Y, Yang X, Wu Z, Guo K, Niu X, Wang Q, Ruan J, Bu W, Gao S. 2017. Two featured series of rRNA-derived RNA fragments (rRFs) constitute a novel class of small RNAs. PLoS ONE 12: e0176458.
Cherlin T, Magee R, Jing Y, Pliatsika V, Loher P, Rigoutsos I. 2020. Ribosomal RNA fragmentation into short RNAs (rRFs) is modulated in a sex- and population of origin-specific manner. BMC Biology 18: 38.
Chery M, Drouard L. 2023. Plant tRNA functions beyond their major role in translation. Journal of Experimental Botany 74: 2352-2363.
Cognat V, Morelle G, Megel C, Lalande S, Molinier J, Vincent T, Small I, Duchêne A-M, Maréchal-Drouard L. 2017. The nuclear and organellar tRNA-derived RNA fragment population in Arabidopsis thaliana is highly dynamic. Nucleic Acids Research 45: 3460-3472.
Cozen AE, Quartley E, Holmes AD, Hrabeta-Robinson E, Phizicky EM, Lowe TM. 2015. ARM-seq: AlkB-facilitated RNA methylation sequencing reveals a complex landscape of modified tRNA fragments. Nature Methods 12: 879-884.
Di Fazio A, Schlackow M, Pong SK, Alagia A, Gullerova M. 2022. Dicer dependent tRNA derived small RNAs promote nascent RNA silencing. Nucleic Acids Research 50: 1734-1752.
Diallo I, Ho J, Lambert M, Benmoussa A, Husseini Z, Lalaouna D, Massé E, Provost P. 2022. A tRNA-derived fragment present in E. coli OMVs regulates host cell gene expression and proliferation. PLoS Pathogens 18: e1010827.
Dunker F, Trutzenberg A, Rothenpieler JS, Kuhn S, Pröls R, Schreiber T, Tissier A, Kemen A, Kemen E, Hückelhoven R et al. 2020. Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence. eLife 9: e56096.
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. Nature Genetics 39: 1033-1037.
Fricker R, Brogli R, Luidalepp H, Wyss L, Fasnacht M, Joss O, Zywicki M, Helm M, Schneider A, Cristodero M et al. 2019. A tRNA half modulates translation as stress response in Trypanosoma brucei. Nature Communications 10: 118.
Gámbaro FL, Calzi M, Fagúndez P, Costa B, Greif G, Mallick E, Lyons S, Ivanov P, Witwer K, Cayota A et al. 2020. Stable tRNA halves can be sorted into extracellular vesicles and delivered to recipient cells in a concentration-dependent manner. RNA Biology 17: 1168-1182.
Ghosal A, Upadhyaya BB, Fritz JV, Heintz-Buschart A, Desai MS, Yusuf D, Huang D, Baumuratov A, Wang K, Galas D et al. 2015. The extracellular RNA complement of Escherichia coli. Microbiology Open 4: 252-266.
Goga A, Stoffel M. 2022. Therapeutic RNA-silencing oligonucleotides in metabolic diseases. Nature Reviews. Drug Discovery 21: 417-439.
Gu H, Lian B, Yuan Y, Kong C, Li Y, Liu C, Qi Y. 2022. A 5' tRNA-Ala-derived small RNA regulates anti-fungal defense in plants. Science China Life Sciences 65: 1-15.
Guan L, Grigoriev A. 2020. Age-related argonaute loading of ribosomal RNA fragments. MicroRNA 9: 142-152.
Guan L, Grigoriev A. 2021. Computational meta-analysis of ribosomal RNA fragments: potential targets and interaction mechanisms. Nucleic Acids Research 49: 4085-4103.
Gupta N, Singh A, Zahra S, Kumar S. 2018. PtRFdb: a database for plant transfer RNA-derived fragments. Database 2018: bay063.
Hackenberg M, Huang P-J, Huang C-Y, Shi B-J, Gustafson P, Langridge P. 2013. A comprehensive expression profile of microRNAs and other classes of non-coding small RNAs in barley under phosphorous-deficient and -sufficient conditions. DNA Research 20: 109-125.
He B, Cai Q, Weiberg A, Li W, Cheng A-P, Ouyang S, Borkovich K, Stajich J, Abreu-Goodger C, Jin H. 2023. Botrytis cinerea small RNAs are associated with tomato AGO1 and silence tomato defense-related target genes supporting cross-kingdom RNAi. bioRxiv. doi: 10.1101/2022.12.30.522274.
Holmes AD, Chan PP, Chen Q, Ivanov P, Drouard L, Polacek N, Kay MA, Lowe TM. 2023. A standardized ontology for naming tRNA-derived RNAs based on molecular origin. Nature Methods 20: 627-628.
Hsieh L-C, Lin S-I, Kuo H-F, Chiou T-J. 2010. Abundance of tRNA-derived small RNAs in phosphate-starved Arabidopsis roots. Plant Signaling & Behavior 5: 537-539.
Hsieh L-C, Lin S-I, Shih AC-C, Chen J-W, Lin W-Y, Tseng C-Y, Li W-H, Chiou T-J. 2009. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151: 2120-2132.
Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. 2011. Angiogenin-induced tRNA fragments inhibit translation initiation. Molecular Cell 43: 613-623.
Kaufmann G. 2000. Anticodon nucleases. Trends in Biochemical Sciences 25: 70-74.
Koeppen K, Hampton TH, Barnaby R, Roche C, Gerber SA, Goo YA, Cho B-K, Vermilyea DM, Hogan DA, Stanton BA. 2023. An rRNA fragment in extracellular vesicles secreted by human airway epithelial cells increases the fluoroquinolone sensitivity of P. aeruginosa. American Journal of Physiology-Lung Cellular and Molecular Physiology 325: L54-L65.
Kumar P, Anaya J, Mudunuri SB, Dutta A. 2014. Meta-analysis of tRNA derived RNA fragments reveals that they are evolutionarily conserved and associate with AGO proteins to recognize specific RNA targets. BMC Biology 12: 78.
Kumar P, Mudunuri SB, Anaya J, Dutta A. 2015. tRFdb: a database for transfer RNA fragments. Nucleic Acids Research 43: D141-D145.
Kusch S, Singh M, Thieron H, Spanu PD, Panstruga R. 2023. Site-specific analysis reveals candidate cross-kingdom small RNAs, tRNA and rRNA fragments, and signs of fungal RNA phasing in the barley-powdery mildew interaction. Molecular Plant Pathology 24: 570-587.
Kuscu C, Kumar P, Kiran M, Su Z, Malik A, Dutta A. 2018. tRNA fragments (tRFs) guide Ago to regulate gene expression post-transcriptionally in a Dicer-independent manner. RNA 24: 1093-1105.
Lalande S, Merret R, Salinas-Giegé T, Drouard L. 2020. Arabidopsis tRNA-derived fragments as potential modulators of translation. RNA Biology 17: 1137-1148.
Lambert M, Benmoussa A, Provost P. 2019. Small non-coding RNAs derived from eukaryotic ribosomal RNA. Non-Coding RNA 5: 16.
Lambert M, Guellal S, Ho J, Benmoussa A, Laffont B, Bélanger R, Provost P. 2022. An expanded landscape of unusually short RNAs in 11 samples from six eukaryotic organisms. Non-Coding RNA 8: 34.
Lambertucci S, Orman KMD, Gupta S, Fisher JP, Gazal S, Williamson RJ, Cramer R, Bindschedler LV. 2019. Analysis of barley leaf epidermis and extrahaustorial proteomes during powdery mildew infection reveals that the PR5 thaumatin-like protein TLP5 is required for susceptibility towards Blumeria graminis f. sp. hordei. Front. Plant Science 10: 953.
Lambertz UO, Ovando ME, Vasconcelos EJR, Unrau PJ, Myler PJ, Reiner NE. 2015. Small RNAs derived from tRNAs and rRNAs are highly enriched in exosomes from both old and new world Leishmania providing evidence for conserved exosomal RNA packaging. BMC Genomics 16: 151.
Lee SR, Collins K. 2005. Starvation-induced cleavage of the tRNA anticodon loop in Tetrahymena thermophila. The Journal of Biological Chemistry 280: 42744-42749.
Lee YS, Shibata Y, Malhotra A, Dutta A. 2009. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes & Development 23: 2639-2649.
Li Y, Gao J, Wang Y, Cai J, Wu D, Wang L, Pu W, Yu F, Zhu S. 2023. The functions of a 5' tRNA-Ala-derived fragment in gene expression. Plant Physiology 193: 1126-1141.
Li Z, Stanton BA. 2021. Transfer RNA-derived fragments, the underappreciated regulatory small RNAs in microbial pathogenesis. Frontiers in Microbiology 12: 687632.
Liu B, Cao J, Wang X, Guo C, Liu Y, Wang T. 2021. Deciphering the tRNA-derived small RNAs: origin, development, and future. Cell Death & Disease 13: 24.
Loss-Morais G, Waterhouse PM, Margis R. 2013. Description of plant tRNA-derived RNA fragments (tRFs) associated with argonaute and identification of their putative targets. Biology Direct 8: 6.
Lucas MC, Pryszcz LP, Medina R, Milenkovic I, Camacho N, Marchand V, Motorin YR, de Pouplana L, Novoa EM. 2023. Quantitative analysis of tRNA abundance and modifications by nanopore RNA sequencing. Nature Biotechnology. doi: 10.1038/s41587-023-01743-6.
Ma X, Liu C, Cao X. 2021a. Plant transfer RNA-derived fragments: biogenesis and functions. Journal of Integrative Plant Biology 63: 1399-1409.
Ma X, Liu C, Kong X, Liu J, Zhang S, Liang S, Luan W, Cao X. 2021b. Extensive profiling of the expressions of tRNAs and tRNA-derived fragments (tRFs) reveals the complexities of tRNA and tRF populations in plants. Science China. Life Sciences 64: 495-511.
Magee R, Rigoutsos I. 2020. On the expanding roles of tRNA fragments in modulating cell behavior. Nucleic Acids Research 48: 9433-9448.
Martinez G. 2018. tRNA-derived small RNAs: new players in genome protection against retrotransposons. RNA Biology 15: 170-175.
Martinez G, Choudury SG, Slotkin RK. 2017. tRNA-derived small RNAs target transposable element transcripts. Nucleic Acids Research 45: 5142-5152.
Masaki H, Ogawa T. 2002. The modes of action of colicins E5 and D, and related cytotoxic tRNases. Biochimie 84: 433-438.
Megel C, Hummel G, Lalande S, Ubrig E, Cognat V, Morelle G, Salinas-Giegé T, Duchêne A-M, Maréchal-Drouard L. 2019. Plant RNases T2, but not Dicer-like proteins, are major players of tRNA-derived fragments biogenesis. Nucleic Acids Research 47: 941-952.
Mukherjee D, Gupta S, Ghosh A, Ghosh A. 2020. Ustilago maydis secreted T2 ribonucleases, Nuc1 and Nuc2 scavenge extracellular RNA. Cellular Microbiology 22: e13256.
Nowacka M, Strozycki PM, Jackowiak P, Hojka-Osinska A, Szymanski M, Figlerowicz M. 2013. Identification of stable, high copy number, medium-sized RNA degradation intermediates that accumulate in plants under non-stress conditions. Plant Molecular Biology 83: 191-204.
Nunes CC, Gowda M, Sailsbery J, Xue M, Chen F, Brown DE, Oh Y, Mitchell TK, Dean RA. 2011. Diverse and tissue-enriched small RNAs in the plant pathogenic fungus, Magnaporthe Oryzae. BMC Genomics 12: 288.
O'Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO. 2020. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nature Reviews. Molecular Cell Biology 21: 585-606.
Pandey KK, Madhry DR, Kumar YS, Malvankar S, Sapra L, Srivastava RK, Bhattacharyya S, Verma B. 2021. Regulatory roles of tRNA-derived RNA fragments in human pathophysiology. Molecular Therapy-Nucleic Acids 26: 161-173.
Park J, Ahn SH, Shin MG, Kim HK, Chang S. 2020. tRNA-derived small RNAs: novel epigenetic regulators. Cancers 12: 2773.
Phizicky EM, Hopper AK. 2010. tRNA biology charges to the front. Genes & Development 24: 1832-1860.
Ren B, Wang X, Duan J, Ma J. 2019. Rhizobial tRNA-derived small RNAs are signal molecules regulating plant nodulation. Science 365: 919-922.
Rossbach O. 2019. Artificial circular RNA sponges targeting microRNAs as a novel tool in molecular biology. Molecular Therapy-Nucleic Acids 17: 452-454.
Scacchetti A, Shields EJ, Trigg NA, Wilusz JE, Conine CC, Bonasio R. 2023. A ligation-independent sequencing method reveals tRNA-derived RNAs with blocked 3′ termini. bioRxiv. doi: 10.1101/2023.06.06.543899.
Sheu-Gruttadauria J, MacRae IJ. 2017. Structural foundations of RNA silencing by Argonaute. Journal of Molecular Biology 429: 2619-2639.
Shi J, Zhang Y, Tan D, Zhang X, Yan M, Zhang Y, Franklin R, Shahbazi M, Mackinlay K, Liu S et al. 2021. PANDORA-seq expands the repertoire of regulatory small RNAs by overcoming RNA modifications. Nature Cell Biology 23: 424-436.
Su Z, Kuscu C, Malik A, Shibata E, Dutta A. 2019. Angiogenin generates specific stress-induced tRNA halves and is not involved in tRF-3-mediated gene silencing. The Journal of Biological Chemistry 294: 16930-16941.
Su Z, Wilson B, Kumar P, Dutta A. 2020. Noncanonical roles of tRNAs: tRNA fragments and beyond. Annual Review of Genetics 54: 47-69.
Sun Z, Hu Y, Zhou Y, Jiang N, Hu S, Li L, Li T. 2022. tRNA-derived fragments from wheat are potentially involved in susceptibility to Fusarium head blight. BMC Plant Biology 22: 3.
Thompson A, Zielezinski A, Plewka P, Szymanski M, Nuc P, Szweykowska-Kulinska Z, Jarmolowski A, Karlowski WM. 2018. tRex: a web portal for exploration of tRNA-derived fragments in Arabidopsis thaliana. Plant & Cell Physiology 59: e1.
Thompson DM, Lu C, Green PJ, Parker R. 2008. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14: 2095-2103.
Thompson DM, Parker R. 2009. The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. The Journal of Cell Biology 185: 43-50.
Tosar JP, Gámbaro F, Darré L, Pantano S, Westhof E, Cayota A. 2018. Dimerization confers increased stability to nucleases in 5′ halves from glycine and glutamic acid tRNAs. Nucleic Acids Research 46: 9081-9093.
Tosar JP, Segovia M, Castellano M, Gámbaro F, Akiyama Y, Fagúndez P, Olivera Á, Costa B, Possi T, Hill M et al. 2020. Fragmentation of extracellular ribosomes and tRNAs shapes the extracellular RNAome. Nucleic Acids Research 48: 12874-12888.
Wang H, Huang R, Li L, Zhu J, Li Z, Peng C, Zhuang X, Lin H, Shi S, Huang P. 2021. CPA-seq reveals small ncRNAs with methylated nucleosides and diverse termini. Cell Discovery 7: 25.
Wang L, Yu X, Wang H, Lu Y-Z, Ruiter M, Prins M, He Y-K. 2011. A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa). BMC Genomics 12: 289.
Wang Q, Li T, Xu K, Zhang W, Wang X, Quan J, Jin W, Zhang M, Fan G, Wang M-B et al. 2016. The tRNA derived small RNAs regulate gene expression through triggering sequence-specific degradation of target transcripts in the oomycete pathogen Phytophthora sojae. Frontiers in Plant Science 7: 1938.
Wang Y, Li H, Sun Q, Yao Y. 2016. Characterization of small RNAs derived from tRNAs, rRNAs and snoRNAs and their response to heat stress in wheat seedlings. PLoS ONE 11: e0150933.
Weiberg A, Wang M, Lin F-M, Zhao H, Zhang Z, Kaloshian I, Huang H-D, Jin H. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342: 118-123.
Weng Q, Wang Y, Xie Y, Yu X, Zhang S, Ge J, Li Z, Ye G, Guo J. 2022. Extracellular vesicles-associated tRNA-derived fragments (tRFs): biogenesis, biological functions, and their role as potential biomarkers in human diseases. Journal of Molecular Medicine 100: 679-695.
Yamasaki S, Ivanov P, Hu G-F, Anderson P. 2009. Angiogenin cleaves tRNA and promotes stress-induced translational repression. The Journal of Cell Biology 185: 35-42.
Yan J, Gu Y, Jia X, Kang W, Pan S, Tang X, Chen X, Tang G. 2012. Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24: 415-427.
Yoshimoto R, Ishida F, Yamaguchi M, Tanaka S. 2022. The production and secretion of tRNA-derived RNA fragments in the corn smut fungus Ustilago maydis. Frontiers in Fungal Biology 3: 958798.
Zagryadskaya EI, Kotlova N, Steinberg SV. 2004. Key elements in maintenance of the tRNA L-shape. Journal of Molecular Biology 340: 435-444.
Zahra S, Singh A, Poddar N, Kumar S. 2021. Transfer RNA-derived non-coding RNAs (tncRNAs): hidden regulation of plants' transcriptional regulatory circuits. Computational and Structural Biotechnology Journal 19: 5278-5291.
Zand Karimi H, Baldrich P, Rutter BD, Borniego L, Zajt KK, Meyers BC, Innes RW. 2022. Arabidopsis apoplastic fluid contains sRNA- and circular RNA-protein complexes that are located outside extracellular vesicles. Plant Cell 34: 1863-1881.
Zhang S, Sun L, Kragler F. 2009. The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation. Plant Physiology 150: 378-387.
Zhu L, Ow DW, Dong Z. 2018. Transfer RNA-derived small RNAs in plants. Science China. Life Sciences 61: 155-161.