CoChat
Sign Up
Cited by 19RNA and protein synthesis mechanismsPlant-Microbe Interactions and ImmunityRNA modifications and cancer

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

The tRNA thiolation-mediated translational control is essential for plant immunity

Open access
Zheng, Xueao, Chen, Hanchen, Deng, Zhiping, Wu, Yujing, Zhong, Linlin, Wu, Chong, Yu, Xiaodan, Chen, Qiansi, Yan, Shunping·2024·eLife
DOI 10.7554/elife.93517PMC PMC10863982

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Plants have evolved sophisticated mechanisms to regulate gene expression to activate immune responses against pathogen infections. However, how the translation system contributes to plant immunity is largely unknown. The evolutionarily conserved thiolation modification of transfer RNA (tRNA) ensures efficient decoding during translation. Here, we show that tRNA thiolation is required for plant immunity in Arabidopsis . We identify a cgb mutant that is hyper-susceptible to the pathogen Pseudomonas syringae. CGB encodes ROL5, a homolog of yeast NCS6 required for tRNA thiolation. ROL5 physically interacts with CTU2, a homolog of yeast NCS2. Mutations in either ROL5 or CTU2 result in loss of tRNA thiolation. Further analyses reveal that both transcriptome and proteome reprogramming during immune responses are compromised in cgb . Notably, the translation of salicylic acid receptor NPR1 is reduced in cgb , resulting in compromised salicylic acid signaling. Our study not only reveals a regulatory mechanism for plant immunity but also uncovers an additional biological function of tRNA thiolation.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.93517

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 74

  1. Agris, 2018, Celebrating wobble decoding: half a century and still much is new, RNA Biology, 15, 537, 10.1080/15476286.2017.1356562 · DOI
  2. Canet, 2010, Structure-function analysis of npr1 alleles in arabidopsis reveals a role for its paralogs in the perception of salicylic acid, Plant, Cell & Environment, 33, 1911, 10.1111/j.1365-3040.2010.02194.x · DOI
  3. Cao, 1997, The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats, Cell, 88, 57, 10.1016/s0092-8674(00)81858-9 · DOI
  4. Chen, 2008, Firefly luciferase complementation imaging assay for protein-protein interactions in plants, Plant Physiology, 146, 368, 10.1104/pp.107.111740 · DOI
  5. Chen, 2021, RAD51 supports DMC1 by inhibiting the SMC5/6 complex during meiosis, The Plant Cell, 33, 2869, 10.1093/plcell/koab136 · DOI
  6. Chen, 2023, The ATR–WEE1 kinase module promotes SUPPRESSOR OF GAMMA RESPONSE 1 translation to activate replication stress responses, The Plant Cell, 35, 3021, 10.1093/plcell/koad126 · DOI
  7. Chen, 2023, Global translational induction during NLR-mediated immunity in plants is dynamically regulated by CDC123, an ATP-sensitive protein, Cell Host & Microbe, 31, 334, 10.1016/j.chom.2023.01.014 · DOI
  8. DeFraia, 2010, Elongator subunit 2 is an accelerator of immune responses in Arabidopsis thaliana, The Plant Journal, 64, 511, 10.1111/j.1365-313X.2010.04345.x · DOI
  9. Defraia, 2013, Elongator subunit 3 positively regulates plant immunity through its histone acetyltransferase and radical S-adenosylmethionine domains, BMC Plant Biology, 13, 10.1186/1471-2229-13-102 · DOI
  10. Delaunay, 2016, Elp3 links tRNA modification to IRES-dependent translation of LEF1 to sustain metastasis in breast cancer, The Journal of Experimental Medicine, 213, 2503, 10.1084/jem.20160397 · DOI
  11. Deng, 2007, A proteomics study of brassinosteroid response in arabidopsis, Molecular & Cellular Proteomics, 6, 2058, 10.1074/mcp.M700123-MCP200 · DOI
  12. Dewez, 2008, The conserved Wobble uridine tRNA thiolase Ctu1-Ctu2 is required to maintain genome integrity, PNAS, 105, 5459, 10.1073/pnas.0709404105 · DOI
  13. Ding, 2018, Opposite roles of salicylic acid receptors npr1 and npr3/npr4 in transcriptional regulation of plant immunity, Cell, 173, 1454, 10.1016/j.cell.2018.03.044 · DOI
  14. Durrant, 2007, Arabidopsis SNI1 and RAD51D regulate both gene transcription and DNA recombination during the defense response, PNAS, 104, 4223, 10.1073/pnas.0609357104 · DOI
  15. Fu, 2012, NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants, Nature, 486, 228, 10.1038/nature11162 · DOI
  16. Hsu, 2016, Super-resolution ribosome profiling reveals unannotated translation events in Arabidopsis, PNAS, 113, E7126, 10.1073/pnas.1614788113 · DOI
  17. Huang, 2005, An early step in wobble uridine tRNA modification requires the elongator complex, RNA, 11, 424, 10.1261/rna.7247705 · DOI
  18. Jablonowski, 2006, tRNAGlu wobble uridine methylation by Trm9 identifies elongator’s key role for zymocin-induced cell death in yeast, Molecular Microbiology, 59, 677, 10.1111/j.1365-2958.2005.04972.x · DOI
  19. Jones, 2006, The plant immune system, Nature, 444, 323, 10.1038/nature05286 · DOI · Paper page
  20. Klassen, 2017, Independent suppression of ribosomal +1 frameshifts by different tRNA anticodon loop modifications, RNA Biology, 14, 1252, 10.1080/15476286.2016.1267098 · DOI
  21. Kumar, 2022, Structural basis of NPR1 in activating plant immunity, Nature, 605, 561, 10.1038/s41586-022-04699-w · DOI
  22. Lahtvee, 2017, Absolute quantification of protein and mrna abundances demonstrate variability in gene-specific translation efficiency in yeast, Cell Systems, 4, 495, 10.1016/j.cels.2017.03.003 · DOI · Paper page
  23. Leiber, 2010, The TOR pathway modulates the structure of cell walls in arabidopsis, The Plant Cell, 22, 1898, 10.1105/tpc.109.073007 · DOI
  24. Leidel, 2009, Ubiquitin-related modifier urm1 acts as a sulphur carrier in thiolation of eukaryotic transfer RNA, Nature, 458, 228, 10.1038/nature07643 · DOI
  25. Leitner, 2015, Meta-regulation of arabidopsis auxin responses depends on tRNA maturation, Cell Reports, 11, 516, 10.1016/j.celrep.2015.03.054 · DOI
  26. Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biology, 15, 10.1186/s13059-014-0550-8 · DOI · Paper page
  27. Lu, 2005, The kluyveromyces lactis gamma-toxin targets tRNA anticodons, RNA, 11, 1648, 10.1261/rna.2172105 · DOI
  28. Mehlgarten, 2010, Elongator function in tRNA wobble uridine modification is conserved between yeast and plants, Molecular Microbiology, 76, 1082, 10.1111/j.1365-2958.2010.07163.x · DOI
  29. Nakai, 2004, Yeast Nfs1p is involved in thio-modification of both mitochondrial and cytoplasmic tRNAs, The Journal of Biological Chemistry, 279, 12363, 10.1074/jbc.M312448200 · DOI
  30. Nakai, 2019, Trna wobble modification affects leaf cell development in Arabidopsis thaliana, Plant & Cell Physiology, 60, 2026, 10.1093/pcp/pcz064 · DOI
  31. Nedialkova, 2015, Optimization of codon translation rates via trna modifications maintains proteome integrity, Cell, 161, 1606, 10.1016/j.cell.2015.05.022 · DOI
  32. Noma, 2009, Mechanistic characterization of the sulfur-relay system for eukaryotic 2-thiouridine biogenesis at tRNA wobble positions, Nucleic Acids Research, 37, 1335, 10.1093/nar/gkn1023 · DOI
  33. Pan, 2018, Modifications and functional genomics of human transfer RNA, Cell Research, 28, 395, 10.1038/s41422-018-0013-y · DOI
  34. Peng, 2021, Salicylic acid: Biosynthesis and signaling, Annual Review of Plant Biology, 72, 761, 10.1146/annurev-arplant-081320-092855 · DOI
  35. Philipp, 2014, The cytosolic thiouridylase CTU2 of Arabidopsis thaliana is essential for posttranscriptional thiolation of tRNAs and influences root development, BMC Plant Biology, 14, 10.1186/1471-2229-14-109 · DOI
  36. Ranjan, 2017, Thio-modification of trna at the wobble position as regulator of the kinetics of decoding and translocation on the ribosome, Journal of the American Chemical Society, 139, 5857, 10.1021/jacs.7b00727 · DOI
  37. Rekhter, 2019, Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid, Science, 365, 498, 10.1126/science.aaw1720 · DOI
  38. Rezgui, 2013, tRNA tKUUU, tQUUG, and tEUUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding, PNAS, 110, 12289, 10.1073/pnas.1300781110 · DOI
  39. Ryals, 1997, The arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B, The Plant Cell, 9, 425, 10.1105/tpc.9.3.425 · DOI
  40. Saleh, 2015, Posttranslational modifications of the master transcriptional regulator npr1 enable dynamic but tight control of plant immune responses, Cell Host & Microbe, 18, 169, 10.1016/j.chom.2015.07.005 · DOI
  41. Schaffrath, 2017, Wobble uridine modifications-a reason to live, a reason to die?!, RNA Biology, 14, 1209, 10.1080/15476286.2017.1295204 · DOI
  42. Sen, 1976, Role of modified nucleosides in tRNA: effect of modification of the 2-thiouridine derivative located at the 5’-end of the anticodon of yeast transfer RNA Lys2, Nucleic Acids Research, 3, 523, 10.1093/nar/3.3.523 · DOI
  43. Shah, 1997, Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene, Molecular Plant-Microbe Interactions, 10, 69, 10.1094/MPMI.1997.10.1.69 · DOI
  44. Shaheen, 2019, Biallelic variants in CTU2 cause DREAM-PL syndrome and impair thiolation of tRNA wobble U34, Human Mutation, 40, 2108, 10.1002/humu.23870 · DOI
  45. Simpson, 2009, Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration, Human Molecular Genetics, 18, 472, 10.1093/hmg/ddn375 · DOI
  46. Spoel, 2009, Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity, Cell, 137, 860, 10.1016/j.cell.2009.03.038 · DOI
  47. Spoel, 2012, How do plants achieve immunity? defence without specialized immune cells, Nature Reviews. Immunology, 12, 89, 10.1038/nri3141 · DOI
  48. Su, 2014, Quantitative analysis of ribonucleoside modifications in tRNA by HPLC-coupled mass spectrometry, Nature Protocols, 9, 828, 10.1038/nprot.2014.047 · DOI
  49. Tada, 2008, Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins, Science, 321, 952, 10.1126/science.1156970 · DOI
  50. Torres, 2014, Role of tRNA modifications in human diseases, Trends in Molecular Medicine, 20, 306, 10.1016/j.molmed.2014.01.008 · DOI
  51. Vlot, 2009, Salicylic acid, a multifaceted hormone to combat disease, Annual Review of Phytopathology, 47, 177, 10.1146/annurev.phyto.050908.135202 · DOI · Paper page
  52. Wang, 2013, The Arabidopsis elongator complex subunit2 epigenetically regulates plant immune responses, The Plant Cell, 25, 762, 10.1105/tpc.113.109116 · DOI
  53. Wang, 2015, Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in arabidopsis in a single generation, Genome Biology, 16, 10.1186/s13059-015-0715-0 · DOI
  54. Wang, 2020, Structural basis of salicylic acid perception by arabidopsis NPR proteins, Nature, 586, 311, 10.1038/s41586-020-2596-y · DOI
  55. Wang, 2022, PABP/purine-rich motif as an initiation module for cap-independent translation in pattern-triggered immunity, Cell, 185, 3186, 10.1016/j.cell.2022.06.037 · DOI
  56. Waszak, 2020, Germline elongator mutations in sonic hedgehog medulloblastoma, Nature, 580, 396, 10.1038/s41586-020-2164-5 · DOI
  57. Wu, 2012, The arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid, Cell Reports, 1, 639, 10.1016/j.celrep.2012.05.008 · DOI
  58. Xu, 2017, uORF-mediated translation allows engineered plant disease resistance without fitness costs, Nature, 545, 491, 10.1038/nature22372 · DOI
  59. Xu, 2020, Natural variations of SLG1 confer high-temperature tolerance in indica rice, Nature Communications, 11, 10.1038/s41467-020-19320-9 · DOI
  60. Yan, 2013, Salicylic acid activates DNA damage responses to potentiate plant immunity, Molecular Cell, 52, 602, 10.1016/j.molcel.2013.09.019 · DOI
  61. Yan, 2014, Perception of the plant immune signal salicylic acid, Current Opinion in Plant Biology, 20, 64, 10.1016/j.pbi.2014.04.006 · DOI
  62. Yoo, 2020, Translational regulation of metabolic dynamics during effector-triggered immunity, Molecular Plant, 13, 88, 10.1016/j.molp.2019.09.009 · DOI
  63. Yu, 2012, clusterProfiler: an R package for comparing biological themes among gene clusters, OMICS, 16, 284, 10.1089/omi.2011.0118 · DOI · Paper page
  64. Yu, 2021, Salicylic acid and ethylene coordinately promote leaf senescence, Journal of Integrative Plant Biology, 63, 823, 10.1111/jipb.13074 · DOI
  65. Yu, 2022, Salicylic acid inhibits gibberellin signaling through receptor interactions, Molecular Plant, 15, 1759, 10.1016/j.molp.2022.10.001 · DOI
  66. Zabel, 2008, Yeast alpha-tubulin suppressor Ats1/Kti13 relates to the elongator complex and interacts with elongator partner protein Kti11, Molecular Microbiology, 69, 175, 10.1111/j.1365-2958.2008.06273.x · DOI
  67. Zavaliev, 2020, Formation of npr1 condensates promotes cell survival during the plant immune response, Cell, 182, 1093, 10.1016/j.cell.2020.07.016 · DOI
  68. Zhang, 2020, A comprehensive online database for exploring ∼20,000 public arabidopsis rna-seq libraries, Molecular Plant, 13, 1231, 10.1016/j.molp.2020.08.001 · DOI
  69. Zheng T. 2022. Cgb project. Software Heritage. swh:1:rev:dc83f7e363376f4364ca5db5000043795eea06c5. https://archive.softwareheritage.org/swh:1:dir:eaa2a2142feb6cd76a512544fe50bff265057dfe;origin=https://github.com/XueaoZHENG/cgb_project;visit=swh:1:snp:243c9307eb31f29b6ac1863ce5d5dfde1b0491f2;anchor=swh:1:rev:dc83f7e363376f4364ca5db5000043795eea06c5.
  70. Zhou, 2020, Plant immunity: danger perception and signaling, Cell, 181, 978, 10.1016/j.cell.2020.04.028 · DOI
  71. Zhou, 2023, Seeing is believing: understanding functions of NPR1 and its paralogs in plant immunity through cellular and structural analyses, Current Opinion in Plant Biology, 73, 10.1016/j.pbi.2023.102352 · DOI
  72. Zinshteyn, 2013, Loss of a conserved tRNA anticodon modification perturbs cellular signaling, PLOS Genetics, 9, 10.1371/journal.pgen.1003675 · DOI
  73. Zheng X, Wu C, Yan S. 2022. The thiolation modification of tRNA is essential for plant immunity. NCBI Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE183087. GSE183087.
  74. Zheng X, Yan S. 2021. The thiolation modification of tRNA is essential for plant immunity. ProteomeXchange. https://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD028189. PXD028189.

Metadata

Authors
Zheng, X., Chen, H., Deng, Z., Wu, Y., Zhong, L., Wu, C., Yu, X., Chen, Q., & Yan, S.
Affiliations
  • Huazhong Agricultural University (CN)
  • ZheJiang Academy of Agricultural Sciences (CN)
  • China Tobacco (CN)
Corresponding author
Yan, Shunping
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2024-01-29
Volume
13
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.93517
PMC
PMC10863982
OpenAlex
W4391322744
Cited by
19
References
1
Citations by year
2026: 8 · 2025: 9 · 2024: 2
FWCI
2.59
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (31970311, 32000373, 32270306)
  • HZAU-AGIS Cooperation Fund (SZYJY2022004)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
Keywords
tRNA thiolation, plant immunity, translational regulation, Pseudomonas syringae, salicylic acid signaling, Arabidopsis thaliana
MeSH terms
Mutation, Plant Diseases, RNA, Transfer, Saccharomyces cerevisiae, Arabidopsis, Gene Expression Regulation, Plant, Salicylic Acid, Arabidopsis Proteins, Plant Immunity

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review