A Negative Feedback Loop Compromises NMD-Mediated Virus Restriction by the Autophagy Pathway in Plants.
SMG7
UPF3
autophagic degradation
nonsense mediated RNA decay
virus restriction
Journal
Advanced science (Weinheim, Baden-Wurttemberg, Germany)
ISSN: 2198-3844
Titre abrégé: Adv Sci (Weinh)
Pays: Germany
ID NLM: 101664569
Informations de publication
Date de publication:
Aug 2024
Aug 2024
Historique:
revised:
21
05
2024
received:
29
01
2024
medline:
27
8
2024
pubmed:
27
8
2024
entrez:
27
8
2024
Statut:
ppublish
Résumé
Nonsense-mediated decay (NMD) and autophagy play pivotal roles in restricting virus infection in plants. However, the interconnection between these two pathways in viral infections has not been explored. Here, it is shown that overexpression of NbSMG7 and NbUPF3 attenuates cucumber green mottle mosaic virus (CGMMV) infection by recognizing the viral internal termination codon and vice versa. NbSMG7 is subjected to autophagic degradation, which is executed by its interaction with one of the autophagy-related proteins, NbATG8i. Mutation of the ATG8 interacting motif (AIM) in NbSMG7 (SMG7mAIM1) abolishes the interaction and comprises its autophagic degradation. Silencing of NbSMG7 and NbATG8i, or NbUPF3 and NbATG8i, compared to silencing each gene individually, leads to more virus accumulations, but overexpression of NbSMG7 and NbATG8i fails to achieve more potent virus inhibition. When CGMMV is co-inoculated with NbSMG7mAIM1 or with NbUPF3, compared to co-inoculating with NbSMG7 in NbATG8i transgene plants, the inoculated plants exhibit milder viral phenotypes. These findings reveal that NMD-mediated virus inhibition is impaired by the autophagic degradation of SMG7 in a negative feedback loop, and a novel regulatory interplay between NMD and autophagy is uncovered, providing insights that are valuable in optimizing strategies to harness NMD and autophagy for combating viral infections.
Identifiants
pubmed: 39189522
doi: 10.1002/advs.202400978
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2400978Subventions
Organisme : National Key Research and Development Program of China
ID : 2021YFD1400400
Organisme : National Natural Science Foundation of China
ID : 32320103010
Informations de copyright
© 2024 The Author(s). Advanced Science published by Wiley‐VCH GmbH.
Références
J. R. Hogg, J. Virol. 2016, 90, 7010.
S. Brogna, T. McLeod, M. Petric, Trends Genet. 2016, 32, 395.
M. Ohtani, A. Wachter, Plant Cell Physiol. 2019, 60, 1953.
I. Szádeczky‐Kardoss, T. Csorba, A. Auber, A. Schamberger, T. Nyikó, J. Taller, T. I. Orbán, J. Burgyán, D. Silhavy, Nucleic Acids Res. 2018, 46, 4632.
I. Szádeczky‐Kardoss, L. Gál, A. Auber, J. Taller, D. Silhavy, Plant Sci 2018, 275, 19.
F. Li, A. Wang, Trends Microbiol. 2019, 27, 792.
A. H. Benkovics, T. Nyikó, Z. Mérai, D. Silhavy, G. D. Bisztray, Plant Mol. Biol. 2011, 75, 277.
O. Shaul, Trends Plant Sci. 2015, 20, 767.
Z. Mérai, A. H. Benkovics, T. Nyikó, M. Debreczeny, L. Hiripi, Z. Kerényi, É. Kondorosi, D. Silhavy, Plant J. 2013, 73, 50.
Y. Dai, W. Li, L. An, Plant Cell Rep. 2016, 35, 5.
D. Garcia, S. Garcia, O. Voinnet, Cell Host Microbe 2014, 16, 391.
G. Balistreri, P. Horvath, C. Schweingruber, D. Zünd, G. McInerney, A. Merits, O. Mühlemann, C. Azzalin, A. Helenius, Cell Host Microbe 2014, 16, 403.
M. Wada, K. G. Lokugamage, K. Nakagawa, K. Narayanan, S. Makino, Proc. Natl. Acad. Sci. USA 2018, 115, E1015.
K. A. Fontaine, K. E. Leon, M. M. Khalid, S. Tomar, D. Jimenez‐Morales, M. Dunlap, J. A. Kaye, P. S. Shah, S. Finkbeiner, N. J. Krogan, M. Ott, mBio 2018, 9, e02126.
L. Ge, B. Cao, R. Qiao, H. Cui, S. Li, H. Shan, P. Gong, M. Zhang, H. Li, A. Wang, X. Zhou, F. Li, Mol. Plant 2023, 16, 632.
H. He, L. Ge, Y. Chen, S. Zhao, Z. Li, X. Zhou, F. Li, Sci China Life Sci 2023, 67, 161.
D. C. Bassham, Curr. Opin. Plant Biol. 2007, 10, 587.
Y. Liu, Y. Xiong, D. C. Bassham, Autophagy 2009, 5, 954.
S. Han, B. Yu, Y. Wang, Y. Liu, Protein Cell 2011, 2, 784.
A. P. Hayward, S. P. Dinesh‐Kumar, Annu. Rev. Phytopathol. 2011, 49, 557.
P. V. Bozhkov, J. Exp. Bot. 2018, 69, 1281.
A. Hafrén, J. L. Macia, A. J. Love, J. J. Milner, M. Drucker, D. Hofius, Proc. Natl. Acad. Sci. USA 2017, 114, E2026.
Y. Haxim, A. Ismayil, Q. Jia, Y. Wang, X. Zheng, T. Chen, L. Qian, N. Liu, Y. Wang, S. Han, J. Cheng, Y. Qi, Y. Hong, Y. Liu, Elife 2017, 6, e23897.
F. Li, M. Zhang, C. Zhang, X. Zhou, New Phytol 2020, 225, 1746.
F. Li, C. Zhang, Y. Li, G. Wu, X. Hou, X. Zhou, A. Wang, Nat. Commun. 2018, 9, 1268.
M. Yang, A. Ismayil, Y. Liu, Annu. Rev. Virol. 2020, 7, 403.
N. K. Kushwaha, A. Hafrén, D. Hofius, Mol. Plant Pathol. 2019, 20, 1211.
M. Yang, Y. Liu, FEBS Lett. 2022, 596, 2152.
B. Cao, L. Ge, M. Zhang, F. Li, X. Zhou, J. Integr. Plant Biol. 2023, 65, 1328.
M. Yang, Y. Zhang, X. Xie, N. Yue, J. Li, X. Wang, C. Han, J. Yu, Y. Liu, D. Li, Plant Cell 2018, 30, 1582.
A. Dombrovsky, L. T. T. Tran‐Nguyen, R. A. C. Jones, Annu. Rev. Phytopathol. 2017, 55, 231.
O. Crespo, D. Janssen, C. García, L. Ruiz, Plant Dis. 2017, 101, 977.
H. H. Tran, B. Chen, H. Chen, R. Menassa, X. Hao, M. Bernards, N. P. A. Hüner, A. Wang, J. Virol. Methods 2019, 269,18.
J. P. May, X. Yuan, E. Sawicki, A. E. Simon, PLoS Pathog. 2018, 14, e1007459.
M. E. Domeier, D. P. Morse, S. W. Knight, M. Portereiko, B. L. Bass, S. E. Mango, Science 2000, 89, 1928.
H. Hori, Y. Watanabe, Plant J. 2005, 43, 530.
L. Arciga‐Reyes, L. Wootton, M. Kieffer, B. Davies, Plant J. 2006, 47, 480.
M. Yoine, T. Nishii, K. Nakamura, Plant Cell Physiol. 2006, 47, 572.
V. K. Raxwal, C. G. Simpson, J. Gloggnitzer, J. C. Entinze, W. Guo, R. Zhang, J. W. S. Brown, K. Riha, Plant Cell 2020, 32, 2725.
C. Capitao, N. Shukla, A. Wandrolova, O. Mittelsten Scheid, K. Riha, Front. Plant Sci. 2018, 9, 1602.
L. Liu, X. Chen, Mol. Plant 2016, 9, 826.
D. C. Baulcombe, Annu. Rev. Virol. 2022, 9, 353.
F. Li, L. Ge, R. Lozano‐Durán, X. Zhou, Trends Microbiol. 2022, 30, 915.
L. Ge, X. Zhou, F. Li, Trends Plant Sci. 2024, 29, 16.
N. Hug, D. Longman, J. F. Cáceres, Nucleic Acids Res. 2016, 44, 1483.
H. W. Jung, G. K. Panigrahi, G. Y. Jung, Y. J. Lee, K. H. Shin, A. Sahoo, E. S. Choi, E. Lee, K. Man Kim, S. H. Yang, J. S. Jeon, S. C. Lee, S. H. Kim, Plant Cell 2020, 32, 1081.
N. Riehs, S. Akimcheva, J. Puizina, P. Bulankova, R. A. Idol, J. Siroky, A. Schleiffer, D. Schweizer, S. D. E. hippen, K. Riha, J. Cell Sci. 2008, 121, 2208.
P. Bulankova, N. Riehs‐Kearnan, M. K. Nowack, A. Schnittger, K. Riha, Plant Cell 2010, 22, 3791.
M. W. Popp, H. Cho, L. E. Maquat, RNA 2020, 26, 1509.
B. Giuseppe, B. Claudia, M. Oliver, Viruses 2017, 9, 24.
N. Lukhovitskaya, L. A. Ryabova, Sci. Rep. 2019, 9, 7042.
J. P. May, P. Z. Johnson, M. Ilyas, F. Gao, A. E. Simon, mBio 2020, 11, e00204.
E. Degtiar, A. Fridman, D. Gottlieb, K. Vexler, I. Berezin, R. Farhi, L. Golani, O. Shaul, Nucleic Acids Res. 2015, 43, 4219.
F. Li, C. Huang, Z. Li, X. Zhou, PLoS Pathog. 2014, 10, e1003921.
F. Li, N. Zhao, Z. Li, X. Xu, Y. Wang, X. Yang, S. S. Liu, A. Wang, X. Zhou, PLoS Pathog. 2017, 13, e1006213.