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PMID: 40036061 Published · epublish English Journal Article

ATG6 interacting with NPR1 increases Arabidopsis thaliana resistance to Pst DC3000/avrRps4 by increasing its nuclear accumulation and stability.

eLife ·Vol. 13 ·2025-03-04

Zhang B, Huang S, Guo S, Meng Y, Tian Y, Zhou Y, Chen H, Li X, Zhou J, Chen W

Abstract

Autophagy-related gene 6 (ATG6) plays a crucial role in plant immunity. Nonexpressor of pathogenesis-related genes 1 (NPR1) acts as a signaling hub of plant immunity. However, the relationship between ATG6 and NPR1 is unclear. Here, we find that ATG6 directly interacts with NPR1. ATG6 overexpression significantly increased nuclear accumulation of NPR1. Furthermore, we demonstrate that ATG6 increases NPR1 protein levels and improves its stability. Interestingly, ATG6 promotes the formation of SINCs (SA-induced NPR1 condensates)-like condensates. Additionally, ATG6 and NPR1 synergistically promote the expression of pathogenesis-related genes. Further results showed that silencing ATG6 in NPR1-GFP exacerbates Pst DC3000/avrRps4 infection, while double overexpression of ATG6 and NPR1 synergistically inhibits Pst DC3000/avrRps4 infection. In summary, our findings unveil an interplay of NPR1 with ATG6 and elucidate important molecular mechanisms for enhancing plant immunity.

Keywords
A. thaliana ATG6 NPR1 Pst DC3000/avrRps4 cell biology cytoplasm nucleus plant biology stability
MeSH Terms
Arabidopsis/microbiology,immunology,genetics Arabidopsis Proteins/metabolism,genetics Plant Diseases/microbiology,immunology Disease Resistance Autophagy-Related Proteins/metabolism,genetics Pseudomonas syringae Cell Nucleus/metabolism Gene Expression Regulation, Plant Protein Binding Protein Stability Plant Immunity
Chemicals
Arabidopsis Proteins NPR1 protein, Arabidopsis Autophagy-Related Proteins
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Zhang Baihong
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Huang Shuqin
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Guo Shuyu
State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, College of Life Sciences, Inner Mongolia University, Hohhot, China. | Key Laboratory of Herbage and Endemic Crop Biotechnology, and College of Life Sciences, Inner Mongolia University, Hohhot, China.
Meng Yixuan
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Tian Yuzhen
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Zhou Yue
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Chen Hang
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Li Xue
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Zhou Jun ORCID
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Chen Wenli ORCID
MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, Guangdong Provincial Key Laboratory of Laser Life Science, Guangzhou Key Laboratory of Spectral Analysis and Functional Probes, College of Biophotonics, School of Optoelectronic Science and Engineering, South China Normal University, Guangzhou, China.
Conflict of Interest

BZ, SH, SG, YM, YT, YZ, HC, XL, JZ, WC No competing interests declared

References (64)
64 references, click to expand
  1. Nuclear localization of NPR1 is required for activation of PR gene expression.
    Plant Cell. 2000 Dec;12(12):2339-2350 PMID: 11148282
  2. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  3. Nuclear targeting in plants.
    Plant Physiol. 1992 Dec;100(4):1627-32 PMID: 16653177
  4. Arabidopsis AtBECLIN 1/AtAtg6/AtVps30 is essential for pollen germination and plant development.
    Cell Res. 2007 Mar;17(3):249-63 PMID: 17339883
  5. Highly specific gene silencing in a monocot species by artificial microRNAs derived from chimeric miRNA precursors.
    Plant J. 2015 Jun;82(6):1061-1075 PMID: 25809382
  6. Six classes of nuclear localization signals specific to different binding grooves of importin alpha.
    J Biol Chem. 2009 Jan 2;284(1):478-485 PMID: 19001369
  7. Gold nanoparticles (AuNPs) can rapidly deliver artificial microRNA (AmiRNA)-ATG6 to silence ATG6 expression in Arabidopsis.
    Plant Cell Rep. 2023 Jul;42(7):1191-1201 PMID: 37160448
  8. Posttranslational Modifications of the Master Transcriptional Regulator NPR1 Enable Dynamic but Tight Control of Plant Immune Responses.
    Cell Host Microbe. 2015 Aug 12;18(2):169-82 PMID: 26269953
  9. Systemic Immunity Requires SnRK2.8-Mediated Nuclear Import of NPR1 in Arabidopsis.
    Plant Cell. 2015 Dec;27(12):3425-38 PMID: 26672073
  10. Engineering Artificial MicroRNAs for Multiplex Gene Silencing and Simplified Transgenic Screen.
    Plant Physiol. 2018 Nov;178(3):989-1001 PMID: 30291175
  11. An estradiol-inducible promoter enables fast, graduated control of gene expression in fission yeast.
    Yeast. 2017 Aug;34(8):323-334 PMID: 28423198
  12. Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance.
    Nat Biotechnol. 2006 Nov;24(11):1420-8 PMID: 17057702
  13. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response.
    Autophagy. 2008 Jan;4(1):20-7 PMID: 17932459
  14. TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis.
    Plant Cell. 2017 Apr;29(4):890-911 PMID: 28351989
  15. Stories of Salicylic Acid: A Plant Defense Hormone.
    Trends Plant Sci. 2020 Jun;25(6):549-565 PMID: 32407695
  16. Bacteria Exploit Autophagy for Proteasome Degradation and Enhanced Virulence in Plants.
    Plant Cell. 2018 Mar;30(3):668-685 PMID: 29500318
  17. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.
    Cell. 1997 Jan 10;88(1):57-63 PMID: 9019406
  18. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens.
    Plant J. 2011 Jun;66(6):953-68 PMID: 21395886
  19. Genetic Analyses of the Arabidopsis ATG1 Kinase Complex Reveal Both Kinase-Dependent and Independent Autophagic Routes during Fixed-Carbon Starvation.
    Plant Cell. 2019 Dec;31(12):2973-2995 PMID: 31615848
  20. Autophagy deficiency leads to accumulation of ubiquitinated proteins, ER stress, and cell death in Arabidopsis.
    Autophagy. 2014 Sep;10(9):1579-87 PMID: 25046116
  21. Chromatin Accessibility Landscape in Human Early Embryos and Its Association with Evolution.
    Cell. 2018 Mar 22;173(1):248-259.e15 PMID: 29526463
  22. Autophagy functions as an antiviral mechanism against geminiviruses in plants.
    Elife. 2017 Feb 28;6: PMID: 28244873
  23. Critical structural elements of the VP16 transcriptional activation domain.
    Science. 1991 Jan 4;251(4989):87-90 PMID: 1846049
  24. Expression of AhDREB1, an AP2/ERF Transcription Factor Gene from Peanut, Is Affected by Histone Acetylation and Increases Abscisic Acid Sensitivity and Tolerance to Osmotic Stress in Arabidopsis.
    Int J Mol Sci. 2018 May 11;19(5): PMID: 29751673
  25. The acidic activation domains of the GCN4 and GAL4 proteins are not alpha helical but form beta sheets.
    Cell. 1993 Feb 26;72(4):587-94 PMID: 8440022
  26. Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness.
    J Exp Bot. 2018 Mar 14;69(6):1415-1432 PMID: 29365132
  27. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants.
    Nature. 2012 May 16;486(7402):228-32 PMID: 22699612
  28. Plant Bax Inhibitor-1 interacts with ATG6 to regulate autophagy and programmed cell death.
    Autophagy. 2017 Jul 3;13(7):1161-1175 PMID: 28537463
  29. Autophagic Degradation of the 26S Proteasome Is Mediated by the Dual ATG8/Ubiquitin Receptor RPN10 in Arabidopsis.
    Mol Cell. 2015 Jun 18;58(6):1053-66 PMID: 26004230
  30. Wheat homologs of yeast ATG6 function in autophagy and are implicated in powdery mildew immunity.
    BMC Plant Biol. 2015 Apr 01;15:95 PMID: 25888209
  31. Abscisic acid promotes proteasome-mediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana.
    Plant J. 2016 Apr;86(1):20-34 PMID: 26865090
  32. Formation of NPR1 Condensates Promotes Cell Survival during the Plant Immune Response.
    Cell. 2020 Sep 3;182(5):1093-1108.e18 PMID: 32810437
  33. Two interacting transcriptional coactivators cooperatively control plant immune responses.
    Sci Adv. 2021 Nov 05;7(45):eabl7173 PMID: 34739308
  34. Nuclear targeting sequences--a consensus?
    Trends Biochem Sci. 1991 Dec;16(12):478-81 PMID: 1664152
  35. Phosphatidylinositol-4-phosphate controls autophagosome formation in Arabidopsis thaliana.
    Nat Commun. 2022 Jul 28;13(1):4385 PMID: 35902598
  36. The amino acid sequence of murine p53 determined from a c-DNA clone.
    Virology. 1984 Apr 30;134(2):477-82 PMID: 6400059
  37. NPR1 Promotes Its Own and Target Gene Expression in Plant Defense by Recruiting CDK8.
    Plant Physiol. 2019 Sep;181(1):289-304 PMID: 31110139
  38. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid.
    Cell Rep. 2012 Jun 28;1(6):639-47 PMID: 22813739
  39. Correlation of Autophagosome Formation with Degradation and Endocytosis Arabidopsis Regulator of G-Protein Signaling (RGS1) through ATG8a.
    Int J Mol Sci. 2019 Aug 27;20(17): PMID: 31461856
  40. An Arabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination.
    Plant Physiol. 2007 Mar;143(3):1132-9 PMID: 17259285
  41. Nucleocytoplasmic transport: signals, mechanisms and regulation.
    Nature. 1997 Apr 24;386(6627):779-87 PMID: 9126736
  42. Nuclear autophagy degrades a geminivirus nuclear protein to restrict viral infection in solanaceous plants.
    New Phytol. 2020 Feb;225(4):1746-1761 PMID: 31621924
  43. Identification of transcription factors that regulate ATG8 expression and autophagy in Arabidopsis.
    Autophagy. 2020 Jan;16(1):123-139 PMID: 30909785
  44. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis.
    Plant Cell. 2009 Sep;21(9):2914-27 PMID: 19773385
  45. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens.
    Plant J. 2011 Jun;66(5):818-30 PMID: 21332848
  46. The NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1) and Related Family: Mechanistic Insights in Plant Disease Resistance.
    Front Plant Sci. 2019 Feb 13;10:102 PMID: 30815005
  47. The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines.
    Plant Cell. 2006 Dec;18(12):3670-85 PMID: 17172357
  48. Construction of gold-siRNA NPR1 nanoparticles for effective and quick silencing of NPR1 in Arabidopsis thaliana.
    RSC Adv. 2020 May 20;10(33):19300-19308 PMID: 35515443
  49. ATG4 Mediated Psm ES4326/AvrRpt2-Induced Autophagy Dependent on Salicylic Acid in Arabidopsis Thaliana.
    Int J Mol Sci. 2020 Jul 21;21(14): PMID: 32708160
  50. Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins.
    Science. 2008 Aug 15;321(5891):952-6 PMID: 18635760
  51. Plant autophagy: mechanisms and functions.
    J Exp Bot. 2018 Mar 14;69(6):1281-1285 PMID: 29547996
  52. Structural basis of NPR1 in activating plant immunity.
    Nature. 2022 May;605(7910):561-566 PMID: 35545668
  53. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  54. Expression of PEI-coated gold nanoparticles carrying exogenous gene in periwinkle mesophyll cells and its practice in huanglongbing research.
    iScience. 2022 May 29;25(6):104479 PMID: 35712078
  55. More stories to tell: NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1, a salicylic acid receptor.
    Plant Cell Environ. 2021 Jun;44(6):1716-1727 PMID: 33495996
  56. Chloroplast Autophagy and Ubiquitination Combine to Manage Oxidative Damage and Starvation Responses.
    Plant Physiol. 2020 Aug;183(4):1531-1544 PMID: 32554506
  57. Transcriptomic and functional analyses reveal an antiviral role of autophagy during pepper mild mottle virus infection.
    BMC Plant Biol. 2020 Oct 29;20(1):495 PMID: 33121441
  58. Multiple Functions of ATG8 Family Proteins in Plant Autophagy.
    Front Cell Dev Biol. 2020 Jun 10;8:466 PMID: 32596242
  59. Autophagy protein 6 (ATG6) is required for pollen germination in Arabidopsis thaliana.
    Autophagy. 2008 Apr;4(3):339-48 PMID: 18227644
  60. Autophagy regulates programmed cell death during the plant innate immune response.
    Cell. 2005 May 20;121(4):567-577 PMID: 15907470
  61. E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses.
    PLoS Genet. 2014 Jan 30;10(1):e1004116 PMID: 24497840
  62. Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1.
    Elife. 2019 Oct 07;8: PMID: 31589140
  63. Beclin1 restricts RNA virus infection in plants through suppression and degradation of the viral polymerase.
    Nat Commun. 2018 Mar 28;9(1):1268 PMID: 29593293
  64. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity.
    Cell. 2009 May 29;137(5):860-72 PMID: 19490895
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Article Info
Journal
eLife
Abbr.
Elife
ISSN
2050-084X
DOI
10.7554/eLife.97206
Published
2025-03-04
Epub
2025-00-04
Language
English
Region
England
NLM ID
101579614
PMCID
PMC11879114
Subset
IM
Grants
National Natural Science Foundation of China · 31570256
External Links
PubMed source DOI: 10.7554/eLife.97206 PMC Full Text View journal details
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