Cytoplasmic and nuclear Sw-5b NLR act both independently and synergistically to confer full host defense against tospovirus infection.
cell-to-cell movement and long-distance movement
cytoplasm
nuclear
nucleotide-binding leucine-rich repeats (NLRs)
plant innate immunity
replication
tomato spotted wilt virus
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
09 2021
09 2021
Historique:
received:
18
01
2021
accepted:
25
05
2021
pubmed:
8
6
2021
medline:
27
8
2021
entrez:
7
6
2021
Statut:
ppublish
Résumé
Plant intracellular nucleotide-binding leucine-rich repeat (NLR) receptors play critical roles in mediating host immunity to pathogen attack. We use tomato Sw-5b::tospovirus as a model system to study the specific role of the compartmentalized plant NLR in dictating host defenses against the virus at different infection steps. We demonstrated here that tomato NLR Sw-5b distributes to the cytoplasm and nucleus, respectively, to play different roles in inducing host resistances against tomato spotted wilt orthotospovirus (TSWV) infection. The cytoplasmic-enriched Sw-5b induces a strong cell death response to inhibit TSWV replication. This host response is, however, insufficient to block viral intercellular and long-distance movement. The nuclear-enriched Sw-5b triggers a host defense that weakly inhibits viral replication but strongly impedes virus intercellular and systemic movement. Furthermore, the cytoplasmic and nuclear Sw-5b act synergistically to dictate a full host defense of TSWV infection. We further demonstrated that the extended N-terminal Solanaceae domain (SD) of Sw-5b plays critical roles in cytoplasm/nucleus partitioning. Sw-5b NLR controls its cytoplasm localization. Strikingly, the SD but not coil-coil domain is crucial for Sw-5b receptor to import into the nucleus to trigger the immunity. The SD was found to interact with importins. Silencing both importin α and β expression disrupted Sw-5b nucleus import and host immunity against TSWV systemic infection. Collectively, our findings suggest that Sw-5b bifurcates disease resistances by cytoplasm/nucleus partitioning to block different infection steps of TSWV. The findings also identified a new regulatory role of extra domain of a plant NLR in mediating host innate immunity.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2262-2281Informations de copyright
© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.
Références
Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
Bai S, Liu J, Chang C, Zhang L, Maekawa T, Wang Q, Xiao W, Liu Y, Chai J, Takken FL et al. 2012. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathogens 8: e1002752.
Bendahmane A, Kanyuka K, Baulcombe DC. 1999. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11: 781-792.
Brommonschenkel SH, Frary A, Frary A, Tanksley SD. 2000. The broad-spectrum tospovirus resistance gene Sw-5 of tomato is a homolog of the root-knot nematode resistance gene Mi. Molecular Plant-Microbe Interactions 13: 1130-1138.
Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP. 2007. A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biology 5: e68.
Canto T, Palukaitis P. 2002. Novel N gene-associated, temperature-independent resistance to the movement of tobacco mosaic virus vectors neutralized by a cucumber mosaic virus RNA1 transgene. Journal of Virology 76: 12908-12916.
Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP. 2008a. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132: 449-462.
Caplan J, Padmanabhan M, Dinesh-Kumar SP. 2008b. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host & Microbe 3: 126-135.
Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN. 2014. A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Frontiers in Plant Science 5: 606.
Cesari S, Moore J, Chen C, Webb D, Periyannan S, Mago R, Bernoux M, Lagudah ES, Dodds PN. 2016. Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC-NLR proteins. Proceedings of the National Academy of Sciences, USA 113: 10204-10209.
Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y et al. 2013. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25: 1463-1481.
Chen T, Liu D, Niu X, Wang J, Qian L, Han L, Liu N, Zhao J, Hong Y, Liu Y. 2017. Antiviral resistance protein Tm-2(2) functions on the plasma membrane. Plant Physiology 173: 2399-2410.
Chen X, Zhu M, Jiang L, Zhao W, Li J, Wu J, Li C, Bai B, Lu G, Chen H et al. 2016. A multilayered regulatory mechanism for the autoinhibition and activation of a plant CC-NB-LRR resistance protein with an extra N-terminal domain. New Phytologist 212: 161-175.
Cheng YT, Germain H, Wiermer M, Bi D, Xu F, Garcia AV, Wirthmueller L, Despres C, Parker JE, Zhang Y et al. 2009. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21: 2503-2516.
Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F, Dangl JL, Epple P. 2010. Arabidopsis type I metacaspases control cell death. Science 330: 1393-1397.
Collier SM, Moffett P. 2009. NB-LRRs work a “bait and switch” on pathogens. Trends in Plant Science 14: 521-529.
Cui H, Tsuda K, Parker JE. 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annual Review of Plant Biology 66: 487-511.
Das B, Sengupta S, Prasad M, Ghose TK. 2014. Genetic diversity of the conserved motifs of six bacterial leaf blight resistance genes in a set of rice landraces. BMC Genetics 15: 82.
De Oliveira AS, Koolhaas I, Boiteux LS, Caldararu OF, Petrescu AJ, Oliveira Resende R, Kormelink R. 2016. Cell death triggering and effector recognition by Sw-5 SD-CNL proteins from resistant and susceptible tomato isolines to tomato spotted wilt virus. Molecular Plant Pathology 17: 1442-1454.
Deom CM, Wolf S, Holt CA, Lucas WJ, Beachy RN. 1991. Altered function of the tobacco mosaic virus movement protein in a hypersensitive host. Virology 180: 251-256.
Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proceedings of the National Academy of Sciences, USA 100: 8024-8029.
Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 11: 539-548.
Engelhardt S, Boevink PC, Armstrong MR, Ramos MB, Hein I, Birch PR. 2012. Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell 24: 5142-5158.
Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW. 2002. The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. The Plant Journal 31: 127-136.
Feng M, Cheng R, Chen M, Guo R, Li L, Feng Z, Wu J, Xie L, Hong J, Zhang Z et al. 2020. Rescue of tomato spotted wilt virus entirely from complementary DNA clones. Proceedings of the National Academy of Sciences, USA 117: 1181-1190.
Feng Z, Xue F, Xu M, Chen X, Zhao W, Garcia-Murria MJ, Mingarro I, Liu Y, Huang Y, Jiang L et al. 2016. The ER-membrane transport system is critical for intercellular trafficking of the NSm movement protein and tomato spotted wilt tospovirus. PLoS Pathogens 12: e1005443.
Gao Z, Chung EH, Eitas TK, Dangl JL. 2011. Plant intracellular innate immune receptor resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. Proceedings of the National Academy of Sciences, USA 108: 7619-7624.
Garcia AV, Blanvillain-Baufume S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE. 2010. Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathogens 6: e1000970.
Gassmann W. 2005. Natural variation in the Arabidopsis response to the avirulence gene hopPsyA uncouples the hypersensitive response from disease resistance. Molecular Plant-Microbe Interactions 18: 1054-1060.
Germain H, Seguin A. 2011. Innate immunity: has poplar made its BED? New Phytologist 189: 678-687.
Hallwass M, de Oliveira AS, de Campos DE, Lohuis D, Boiteux LS, Inoue-Nagata AK, Resende RO, Kormelink R. 2014. The tomato spotted wilt virus cell-to-cell movement protein (NSm) triggers a hypersensitive response in Sw-5-containing resistant tomato lines and in Nicotiana benthamiana transformed with the functional Sw-5b resistance gene copy. Molecular Plant Pathology 15: 871-880.
Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE. 2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334: 1401-1404.
Heinlein M. 2015. Plant virus replication and movement. Virology 479-480: 657-671.
Horsefield S, Burdett H, Zhang X, Manik MK, Shi Y, Chen J, Qi T, Gilley J, Lai JS, Rank MX et al. 2019. NAD+ cleavage activity by animal and plant TIR domains in cell death pathways. Science 365: 793-799.
Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A, Sugano S, Jiang CJ, Takatsuji H. 2013. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proceedings of the National Academy of Sciences, USA 110: 9577-9582.
Jones JD, Vance RE, Dangl JL. 2016. Intracellular innate immune surveillance devices in plants and animals. Science 354: aaf6395.
Kanneganti TD, Bai X, Tsai CW, Win J, Meulia T, Goodin M, Kamoun S, Hogenhout SA. 2007. A functional genetic assay for nuclear trafficking in plants. The Plant Journal 50: 149-158.
Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, Fournier E, Tharreau D, Terauchi R. 2012. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. The Plant Journal 72: 894-907.
Kapos P, Devendrakumar KT, Li X. 2019. Plant NLRs: from discovery to application. Plant Science 279: 3-18.
Katagiri F, Tsuda K. 2010. Understanding the plant immune system. Molecular Plant-Microbe Interactions 23: 1531-1536.
Kawano Y, Fujiwara T, Yao A, Housen Y, Hayashi K, Shimamoto K. 2014. Palmitoylation-dependent membrane localization of the rice resistance protein pit is critical for the activation of the small GTPase OsRac1. Journal of Biological Chemistry 289: 19079-19088.
Kong L, Qiu X, Kang J, Wang Y, Chen H, Huang J, Qiu M, Zhao Y, Kong G, Ma Z et al. 2017. A Phytophthora effector manipulates host histone acetylation and reprograms defense gene expression to promote infection. Current Biology 27: 981-991.
Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL. 2011. Negative-strand RNA viruses: the plant-infecting counterparts. Virus Research 162: 184-202.
Kourelis J, van der Hoorn RAL. 2018. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30: 285-299.
Kroj T, Chanclud E, Michel-Romiti C, Grand X, Morel JB. 2016. Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytologist 210: 618-626.
Lanford RE, Butel JS. 1984. Construction and characterization of an SV40 mutant defective in nuclear transport of T antigen. Cell 37: 801-813.
Lapin D, Bhandari DD, Parker JE. 2020. Origins and immunity networking functions of EDS1 family proteins. Annual Review of Phytopathology 58: 253-276.
Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D, Kraut A, Zhou B, Levaillant M, Adachi H, Yoshioka H et al. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161: 1074-1088.
Leastro MO, Pallas V, Resende RO, Sanchez-Navarro JA. 2017. The functional analysis of distinct tospovirus movement proteins (NSm) reveals different capabilities in tubule formation, cell-to-cell and systemic virus movement among the tospovirus species. Virus Research 227: 57-68.
Li J, Huang H, Zhu M, Huang S, Zhang W, Dinesh-Kumar SP, Tao X. 2019. A plant immune receptor adopts a two-step recognition mechanism to enhance viral effector perception. Molecular Plant 12: 248-262.
Li W, Zhao Y, Liu C, Yao G, Wu S, Hou C, Zhang M, Wang D. 2012. Callose deposition at plasmodesmata is a critical factor in restricting the cell-to-cell movement of soybean mosaic virus. Plant Cell Reports 31: 905-916.
Li X, Kapos P, Zhang Y. 2015. NLRs in plants. Current Opinion in Immunology 32: 114-121.
Lopez C, Aramburu J, Galipienso L, Soler S, Nuez F, Rubio L. 2011. Evolutionary analysis of tomato Sw-5 resistance-breaking isolates of tomato spotted wilt virus. Journal of General Virology 92(Pt 1): 210-215.
Lucas WJ. 2006. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344: 169-184.
Lukasik-Shreepaathy E, Slootweg E, Richter H, Goverse A, Cornelissen BJ, Takken FL. 2012. Dual regulatory roles of the extended N terminus for activation of the tomato Mi-1.2 resistance protein. Molecular Plant-Microbe Interactions 25: 1045-1057.
Ma S, Lapin D, Liu L, Sun Y, Song W, Zhang X, Logemann E, Yu D, Wang J, Jirschitzka J et al. 2020. Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science 370: eabe3069.
Ma Y, Guo H, Hu L, Martinez PP, Moschou PN, Cevik V, Ding P, Duxbury Z, Sarris PF, Jones JDG. 2018. Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors. Proceedings of the National Academy of Sciences, USA 115: 10218-10227.
Ma Z, Song T, Zhu L, Ye W, Wang Y, Shao Y, Dong S, Zhang Z, Dou D, Zheng X et al. 2015. A Phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. Plant Cell 27: 2057-2072.
Ma Z, Zhu L, Song T, Wang Y, Zhang Q, Xia Y, Qiu M, Lin Y, Li H, Kong L et al. 2017. A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 355: 710-714.
Meier N, Hatch C, Nagalakshmi U, Dinesh-Kumar SP. 2019. Perspectives on intracellular perception of plant viruses. Molecular Plant Pathology 20: 1185-1190.
Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. 2003. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809-834.
Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10: 1307-1319.
Mittler R, Herr EH, Orvar BL, van Camp W, Willekens H, Inze D, Ellis BE. 1999. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proceedings of the National Academy of Sciences, USA 96: 14165-14170.
Oliver JE, Whitfield AE. 2016. The genus tospovirus: emerging bunyaviruses that threaten food security. Annual Review of Virology 3: 101-124.
Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. 2013. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathogens 9: e1003235.
Palma K, Zhang Y, Li X. 2005. An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Current Biology 15: 1129-1135.
Peiro A, Canizares MC, Rubio L, Lopez C, Moriones E, Aramburu J, Sanchez-Navarro J. 2014. The movement protein (NSm) of tomato spotted wilt virus is the avirulence determinant in the tomato Sw-5 gene-based resistance. Molecular Plant Pathology 15: 802-813.
Qi D, DeYoung BJ, Innes RW. 2012. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiology 158: 1819-1832.
Qi D, Innes RW. 2013. Recent advances in plant NLR structure, function, localization, and signaling. Frontiers in Immunology 4: 348.
Rao ALN, Choi YG. 2002. Molecular biology of plant virus movement. In: Khan J, Dijkstra J, eds. Plant viruses as molecular pathogens. Boca Raton, FL, USA: CRC Press, Chapter 7.
Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV. 2016. Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biology 14: 8.
Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J, Derbyshire P, Cevik V, Rallapalli G, Saucet SB et al. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161: 1089-1100.
Scholthof KB, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P et al. 2011. Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology 12: 938-954.
Seo JK, Kwon SJ, Cho WK, Choi HS, Kim KH. 2014. Type 2C protein phosphatase is a key regulator of antiviral extreme resistance limiting virus spread. Scientific Reports 4: 5905.
Seong K, Seo E, Witek K, Li M, Staskawicz B. 2020. Evolution of NLR resistance genes with noncanonical N-terminal domains in wild tomato species. New Phytologist 227: 1530-1543.
Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P. 2007. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098-1103.
Slootweg E, Roosien J, Spiridon LN, Petrescu AJ, Tameling W, Joosten M, Pomp R, van Schaik C, Dees R, Borst JW et al. 2010. Nucleocytoplasmic distribution is required for activation of resistance by the potato NB-LRR receptor Rx1 and is balanced by its functional domains. Plant Cell 22: 4195-4215.
Soosaar JL, Burch-Smith TM, Dinesh-Kumar SP. 2005. Mechanisms of plant resistance to viruses. Nature Reviews Microbiology 3: 789-798.
Spassova MI, Prins TW, Folkertsma RT, Klein-Lankhorst RM, Hille J, Goldbach RW, Prins M. 2001. The tomato gene Sw-5 is a member of the coiled coil, nucleotide binding, leucine-rich repeat class of plant resistance genes and confers resistance to TSWV in tobacco. Molecular Breeding 7: 151.
Stewart M. 2007. Molecular mechanism of the nuclear protein import cycle. Nature Reviews Molecular Cell Biology 8: 195-208.
Takemoto D, Rafiqi M, Hurley U, Lawrence GJ, Bernoux M, Hardham AR, Ellis JG, Dodds PN, Jones DA. 2012. N-terminal motifs in some plant disease resistance proteins function in membrane attachment and contribute to disease resistance. Molecular Plant-Microbe Interactions 25: 379-392.
Taliansky M, Torrance L, Kalinina NO. 2008. Role of plant virus movement proteins. Methods in Molecular Biology 451: 33-54.
Tameling WI, Nooijen C, Ludwig N, Boter M, Slootweg E, Goverse A, Shirasu K, Joosten MH. 2010. RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell 22: 4176-4194.
Tasset C, Bernoux M, Jauneau A, Pouzet C, Briere C, Kieffer-Jacquinod S, Rivas S, Marco Y, Deslandes L. 2010. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLoS Pathogens 6: e1001202.
Van Der Biezen EA, Jones JDG. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends in Biochemical Sciences 23: 454-456.
Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M et al. 1998. The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nature Biotechnology 16: 1365-1369.
van der Vossen EA, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S. 2005. The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. The Plant Journal 44: 208-222.
Vossen JH, van Arkel G, Bergervoet M, Jo KR, Jacobsen E, Visser RG. 2016. The Solanum demissum R8 late blight resistance gene is an Sw-5 homologue that has been deployed worldwide in late blight resistant varieties. Theoretical and Applied Genetics 129: 1785-1796.
Wang A. 2015. Dissecting the molecular network of virus-plant interactions: the complex roles of host factors. Annual Review of Phytopathology 53: 45-66.
Wang J, Chen T, Han M, Qian L, Li J, Wu M, Han T, Cao J, Nagalakshmi U, Rathjen JP et al. 2020. Plant NLR immune receptor Tm-22 activation requires NB-ARC domain-mediated self-association of CC domain. PLoS Pathogens 16: e1008475.
Wang J, Hu M, Wang J, Qi J, Han Z, Wang G, Qi Y, Wang HW, Zhou JM, Chai J. 2019a. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364: eaav5870.
Wang J, Wang J, Hu M, Wu S, Qi J, Wang G, Han Z, Qi Y, Gao N, Wang HW et al. 2019b. Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364: eaav5868.
Wen W, Meinkoth JL, Tsien RY, Taylor SS. 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell 82: 463-473.
van Wersch S, Tian L, Hoy R, Li X. 2020. Plant NLRs: the whistleblowers of plant immunity. Plant Communications 1: 100016.
Wirthmueller L, Zhang Y, Jones JD, Parker JE. 2007. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Current Biology 17: 2023-2029.
Zhang Y, Li X. 2005. A putative nucleoporin 96 is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1, constitutive 1. Plant Cell 17: 1306-1316.
Zhao W, Jiang L, Feng Z, Chen X, Huang Y, Xue F, Huang C, Liu Y, Li F, Liu Y et al. 2016. Plasmodesmata targeting and intercellular trafficking of tomato spotted wilt tospovirus movement protein NSm is independent of its function in HR induction. Journal of General Virology 97: 1990-1997.
Zhu M, van Grinsven IL, Kormelink R, Tao X. 2019. Paving the way to tospovirus infection: multilined interplays with plant innate immunity. Annual Review of Phytopathology 57: 41-62.
Zhu M, Jiang L, Bai B, Zhao W, Chen X, Li J, Liu Y, Chen Z, Wang B, Wang C et al. 2017. The intracellular immune receptor Sw-5b confers broad-spectrum resistance to tospoviruses through recognition of a conserved 21-amino acid viral effector epitope. Plant Cell 29: 2214-2232.