The NSm proteins of phylogenetically related tospoviruses trigger Sw-5b–mediated resistance dissociated of their cell-to-cell movement function

Leastro, Mikhail Oliveira; Oliveira, A. S. de; Pallás, Vicente; Sánchez‐Navarro, J. A.; Kormelink, Richard; Resende, Renato O.

doi:10.1016/j.virusres.2017.07.019

Cited by 15 publications

(19 citation statements)

References 26 publications

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“…During HR, infected and neighboring cells are thought to kill themselves to halt the pathogen spread throughout the plant tissue. While the Sw-5b -transformed N. tabacum plants do not show any HR after mechanical inoculation with TSWV ( Spassova et al, 2001 ), and strengthen the concept that the HR is not the resistance mechanism of NB-LRR proteins ( Liu et al, 2010 ), the Sw-5b gene-transformed N. benthamiana plants show a clear, concomitant HR ( Hallwass et al, 2014 ; Leastro et al, 2017 ). The main difference between these two transgenic plants is that in N. tabacum expression of the Sw-5b gene is governed by its own regulatory sequences ( Spassova et al, 2001 ) while in N. benthamiana the Sw-5b gene is driven by constitutive expression from the strong 35S promoter of cauliflower mosaic virus ( Hallwass et al, 2014 ).…”

Section: Hypersensitive Cell Death Response Triggered By Sw-5bmentioning

confidence: 87%

“…More recently, N. benthamiana plants transformed with the Sw-5b gene copy were challenged with six different orthotospoviruses. Besides the aforementioned four orthotospoviruses, Sw-5b provided resistance to alstroemeria necrotic streak virus (ANSV) and impatiens necrotic spot virus (INSV) as well ( Leastro et al, 2017 ). Thus, the Sw-5b gene alone is sufficient for broad-spectrum resistance, although this applies to phylogenetically related orthotospoviruses that are clustered in the same evolutionary clade ( de Oliveira et al, 2012 ; Lima et al, 2016 ).…”

Section: Discovery Of the Sw-5 Gene Clustermentioning

confidence: 99%

“…Final evidence for the identification of the avr-determinant came from transient expression analysis of TSWV proteins from binary clones using agrobacteria, in which only NSm triggered HR in plants harboring a functional Sw-5b gene copy ( Hallwass et al, 2014 ; Peiro et al, 2014 ). Moreover, expression of NSm proteins from CSNV and TCSV isolates also triggered HR in those plants, being abrogated by the introduction of mutations C118Y or T120N ( Leastro et al, 2017 ). All these experiments validated NSm as the avr-determinant of Sw-5b.…”

Section: Identification Of the Avr-determinant/effector Of Sw-5bmentioning

confidence: 99%

“…(a wild Peruvian tomato), revealed five paralogs, the so-called Sw-5 gene cluster ( Spassova et al, 2001 ). Isolation of two resistance gene candidates (RGCs) and their subsequent transformation into tobacco plants helped to demonstrate that the gene copy Sw-5b is solely responsible for a broad-spectrum resistance to orthotospoviruses ( Spassova et al, 2001 ; Hallwass et al, 2014 ; Leastro et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

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The Sw-5 Gene Cluster: Tomato Breeding and Research Toward Orthotospovirus Disease Control

et al. 2018

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The Sw-5 gene cluster encodes protein receptors that are potentially able to recognize microbial products and activate signaling pathways that lead to plant cell immunity. Although there are several Sw-5 homologs in the tomato genome, only one of them, named Sw-5b, has been extensively studied due to its functionality against a wide range of (thrips-transmitted) orthotospoviruses. The Sw-5b gene is a dominant resistance gene originally from a wild Peruvian tomato that has been used in tomato breeding programs aiming to develop cultivars with resistance to these viruses. Here, we provide an overview starting from the first reports of Sw-5 resistance, positional cloning and the sequencing of the Sw-5 gene cluster from resistant tomatoes and the validation of Sw-5b as the functional protein that triggers resistance against orthotospoviruses. Moreover, molecular details of this plant–virus interaction are also described, especially concerning the roles of Sw-5b domains in the sensing of orthotospoviruses and in the signaling cascade leading to resistance and hypersensitive response.

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Section: Hypersensitive Cell Death Response Triggered By Sw-5bmentioning

confidence: 87%

Section: Discovery Of the Sw-5 Gene Clustermentioning

confidence: 99%

Section: Identification Of the Avr-determinant/effector Of Sw-5bmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Sw-5 Gene Cluster: Tomato Breeding and Research Toward Orthotospovirus Disease Control

et al. 2018

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“…Orthotospovirus NSm protein facilitates the movement of viral ribonucleoproteins from cell-to-cell. NSm of TSWV has recently been identified as the avirulence factor recognized by the product of resistance gene Sw - 5b from tomato ( Solanum lycopersicum L.) [10]. The S RNA segment is of negative polarity in members of the genera Orthobunyavirus , Orthohantavirus and Orthonairovirus , and ambisense in members of the genera Phlebovirus and Orthotospovirus .…”

Section: Introductionmentioning

confidence: 99%

The bunyavirus nonstructural protein NSs suppresses plant immunity to facilitate its own transmission by improving vector insect performance

Zhao

et al. 2018

Preprint

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15Pandemics of vector-borne human and plant pathogens often rely on the behaviors of 16 their arthropod vectors. Arboviruses, including many bunyaviruses, manipulate vector 17 behavior to accelerate their own transmission to vertebrates, birds, insects, and plants. 18 However, the molecular mechanism underlying this manipulation remains elusive. 19 Here, we report that the non-structural protein NSs of orthotospovirus (order 20 Bunyavirales, family Tospoviridae), is a key viral factor that indirectly modifies 21 vector preference and increases vector performance. NSs suppresses the biosynthesis 22 of volatile monoterpenes, which serve as repellents of the vector Western flower 23 thrips (WFT, Frankliniella occidentalis) instead of using its known silencing 24 suppressor activity. NSs directly interacts with and relocalizes the jasmonate (JA) 25 signaling master regulator MYC2 and its two close homologs, MYC3 and MYC4, to 26 disable JA-mediated activation of terpene synthase genes. The dysfunction of the 27 MYCs subsequently attenuates host defenses, increases the attraction of thrips, and 2 28 improves thrips fitness. These findings elucidate the molecular mechanism through 29 which a bunyavirus manipulates vector behaviors and therefore facilitate disease 30 transmission. Our results provide important insights into the molecular mechanisms 31 by which tospoviruses NSs counteracts host immunity for pathogen transmission. 32 Author summary 33 Most bunyaviruses are transmitted by insect vectors, and some of them can modify 34 the behaviors of their arthropod vectors to increase transmission to mammals, birds, 35 and plants. NSs is a non-structural bunyavirus protein with multiple functions that 36 acts as an avirulence determinant and silencing suppressor. In this study, we identified 37 a new function of NSs as a manipulator of vector behavior, independent of its 38 silencing suppressor activity. NSs manipulates jasmonate-mediated immunity against 39 thrips by directly interacting with several homologs of MYC transcription factors, the 40 core regulators of the jasmonate-signaling pathway. This hijacking by NSs enhances 41 thrips preference and performance. Many human-and animal-infecting members of 42the Bunyaviridales also encode NSs and could manipulate vector behavior to 43 accelerate their own transmission. Therefore, our data support the hypothesis that the 44 NSs protein may play conserved roles among various members of the Bunyaviridales 45 in the modification of vector feeding behavior that evolved as a mechanism to 46 enhance virus transmission. 47 48 Arthropod-borne viruses (arboviruses) are virulent causal agents of diseases in 49 humans, animals, and plants. Vector behaviors have critical ecological and 50 evolutionary consequences for arboviruses, which rely exclusively on their arthropod 51 vectors for dispersal to (and survival in) new hosts. Therefore, it is of evolutionary 3 52 significance for an arbovirus to alter its vector's behavior to facilitate its own 53 transmission. Interestingly,...

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Plant Viruses of Agricultural Importance: Current and Future Perspectives of Virus Disease Management Strategies

Satyanarayana

Hein

2023

Phytopathology®

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Plant viruses cause significant losses in agricultural crops worldwide, affecting the yield and quality of agricultural products. The emergence of novel viruses or variants through genetic evolution and spillover from reservoir host species, changes in agricultural practices, mixed infections with disease synergism, and impacts from global warming pose continuous challenges for the management of epidemics resulting from emerging plant virus diseases. This review describes some of the most devastating virus diseases plus select virus diseases with regional importance in agriculturally important crops that have caused significant yield losses. The lack of curative measures for plant virus infections prompts the use of risk-reducing measures for managing plant virus diseases. These measures have included exclusion, avoidance, and eradication techniques, along with vector management practices. The advent of Next-Generation Sequencing technologies has great potential for detecting unknown viruses in quarantine samples. The deployment of genetic resistance in crop plants is an effective and desirable method of managing virus diseases. Several dominant and recessive resistance genes have been used to manage virus diseases in crops. Recently, RNA-based technologies such as dsRNA- and siRNA-based RNA interference, microRNA, and CRISPR/Cas9 provide transgenic and non-transgenic approaches for developing virus-resistant crop plants. Importantly, the topical application of dsRNA, hairpin RNA, and artificial microRNA and trans-active siRNA molecules on plants has the potential to develop GMO-free virus disease management methods. However, the long-term efficacy and acceptance of these new technologies, especially transgenic methods, remain to be established

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The NSm proteins of phylogenetically related tospoviruses trigger Sw-5b–mediated resistance dissociated of their cell-to-cell movement function

Cited by 15 publications

References 26 publications

The Sw-5 Gene Cluster: Tomato Breeding and Research Toward Orthotospovirus Disease Control

The Sw-5 Gene Cluster: Tomato Breeding and Research Toward Orthotospovirus Disease Control

The bunyavirus nonstructural protein NSs suppresses plant immunity to facilitate its own transmission by improving vector insect performance

Plant Viruses of Agricultural Importance: Current and Future Perspectives of Virus Disease Management Strategies

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